V. CYCLOSTOMATA[23]
[23] The following classification of the Cyclostomata is employed in the present chapter:
I. Hyperoartia ex. Petromyzon. II. Hyperotreta ex. Myxine, Bdellostoma.
Petromyzon is the only type of this degenerated but primitive group of Fishes the development of which has been as yet studied[24].
[24] The present chapter is in the main founded upon observations which I was able to make in the spring of 1880 upon the development of Petromyzon Planeri. Mr Scott very kindly looked over my proof-sheets and made a number of valuable suggestions, and also sent me an early copy of his preliminary note (No. 87), which I have been able to make use of in correcting my proof-sheets.
The development does not however throw any light on the relationships of the group. The similarity of the mouth and other parts of Petromyzon to those of the Tadpole probably indicates that there existed a common ancestral form for the Cyclostomata and Amphibia. Embryology does not however add anything to the anatomical evidence on this subject. The fact of the segmentation being complete was at one time supposed to indicate an affinity between the two groups; but the discovery that the segmentation is also complete in the Ganoids deprives this feature in the development of any special weight. In the formation of the layers and in most other developmental characters there is nothing to imply a special relationship with the Amphibia, and in the mode of formation of the nervous system Petromyzon exhibits a peculiar modification, otherwise only known to occur in Teleostei and Lepidosteus.
Dohrn[25] was the first to bring into prominence the degenerate character of the Cyclostomata. I cannot however assent to his view that they are descended from a relatively highly-organized type of Fish. It appears to me almost certain that they belong to a group of fishes in which a true skeleton of branchial bars had not become developed, the branchial skeleton they possess being simply an extra-branchial system; while I see no reason to suppose that a true branchial skeleton has disappeared. If the primitive Cyclostomata had not true branchial bars, they could not have had jaws, because jaws are essentially developed from the mandibular branchial bar. These considerations, which are supported by numerous other features of their anatomy, such as the character of the axial skeleton, the straightness of the intestinal tube, the presence of a subintestinal vein etc., all tend to prove that these fishes are remnants of a primitive and prægnathostomatous group. The few surviving members of the group have probably owed their preservation to their parasitic or semiparasitic habits, while the group as a whole probably disappeared on the appearance of gnathostomatous Vertebrata.
[25] Der Ursprung d. Wirbelthiere, etc. Leipzig, 1875.
The ripe ovum of Petromyzon Planeri is a slightly oval body of about 1 mm. in diameter. It is mainly formed of an opaque nearly white yolk, invested by a membrane composed of an inner perforated layer, and an outer structureless layer. There appears to be a pore perforating the inner layer at the formative pole, which may be called a micropyle (Kupffer and Benecke, No. 79). Enclosing the egg-membranes there is present a mucous envelope, which causes the egg, when laid, to adhere to stones or other objects.
[FIG. 37. LONGITUDINAL VERTICAL SECTION THROUGH AN EMBRYO OF PETROMYZON PLANERI OF 136 HOURS.
me. mesoblast; yk. yolk-cells; al. alimentary tract; bl. blastopore; s.c. segmentation cavity.]
Impregnation is effected by the male attaching itself by its suctorial mouth to the female. The attached couple then shake together; and, as they do so, they respectively emit from their abdominal pores ova and spermatozoa which pass into a hole previously made[26].
[26] Artificial impregnation may be effected without difficulty by squeezing out into the same vessel the ova and spermatozoa of a ripe female and male. The fertilized eggs are easily reared. Petromyzon Planeri breeds during the second half of April.
The segmentation is total and unequal, and closely resembles that in the Frog's egg (Vol. II. p. 96). The upper pole is very slightly whiter than the lower. A segmentation cavity is formed very early, and is placed between the small cells of the upper pole and the large cells of the lower pole. It is proportionately larger than in the Frog; and the roof eventually thins out so as to be formed of a single row of small cells. At the sides of the segmentation cavity there are always several rows of small cells, which gradually merge into the larger cells of the lower pole of the egg. The segmentation is completed in about fifty hours.
[FIG. 38. TRANSVERSE SECTION THROUGH A PETROMYZON EMBRYO 160 HOURS AFTER IMPREGNATION.
ep. epiblast; al. mesenteron; yk. yolk-cells; ms. mesoblast.]
The segmentation is followed by an asymmetrical invagination (fig. 37) which leads to a mode of formation of the hypoblast fundamentally similar to that in the Frog. The process has been in the main correctly described by M. Schultze (No. 81).
On the border between the large and small cells of the embryo, at a point slightly below the segmentation cavity, a small circular pit appears; the roof of which is formed by an infolding of the small cells, while the floor is formed of the large cells. This pit is the commencing mesenteron. It soon grows deeper (fig. 37, al) and extends as a well-defined tube (shewn in transverse section in fig. 38, al) in the direction of the segmentation cavity. In the course of the formation of the mesenteron the segmentation cavity gradually becomes smaller, and is finally (about the 200th hour) obliterated. The roof of the mesenteron is formed by the continued invagination of small cells, and its floor is composed of large yolk-cells. The wide external opening is arched over dorsally by a somewhat prominent lip--the homologue of the embryonic rim. The opening persists till nearly the time of hatching; but eventually becomes closed, and is not converted into the permanent anus. On the formation of the mesenteron the hypoblast is composed of two groups of cells, (1) the yolk-cells, and (2) the cells forming the roof of the mesenteron.
While the above changes are taking place, the small cells, or as they may now be called the epiblast cells, gradually spread over the large yolk-cells, as in normal types of epibolic invagination. The growth over the yolk-cells is not symmetrical, but is most rapid in the meridian opposite the opening of the alimentary cavity, so that the latter is left in a bay (cf. Elasmobranchii, p. 63). The epibolic invagination takes place as in Molluscs and many other forms, not simply by the division of pre-existing epiblast cells, but by the formation of fresh epiblast cells from the yolk-cells (fig. 37); and till after the complete enclosure of the yolk-cells there is never present a sharp line of demarcation between the two groups of cells. By the time that the segmentation cavity is obliterated the whole yolk is enclosed by the epiblast. The yolk-cells adjoining the opening of the mesenteron are the latest to be covered in, and on their enclosure this opening constitutes the whole of the blastopore. The epiblast is composed of a single row of columnar cells.
Mesoblast and notochord. During the above changes the mesoblast becomes established. It arises, as in Elasmobranchs, in the form of two plates derived from the primitive hypoblast. During the invagination to form the mesenteron some of the hypoblast cells on each side of the invaginated layer become smaller, and marked off as two imperfect plates (fig. 38, ms). It is difficult to say whether these plates are entirely derived from invaginated cells, or are in part directly formed from the pre-existing yolk-cells, but I am inclined to adopt the latter view; the ventral extension of the mesoblast plates undoubtedly takes place at the expense of the yolk-cells. The mesoblast plates soon become more definite, and form (fig. 39, ms) well-defined structures, triangular in section, on the two sides of the middle line.
[FIG. 39. TRANSVERSE SECTION THROUGH AN EMBRYO OF PETROMYZON PLANERI OF 208 HOURS.
The figure illustrates the formation of the neural cord and of the notochord.
ms. mesoblast; nc. neural cord; ch. notochord; yk. yolk-cells; al. alimentary canal.]
At the time the mesoblast is first formed the hypoblast cells, which roof the mesenteron, are often imperfectly two layers thick (fig. 38). They soon however become constituted of a single layer only. When the mesoblast is fairly established, the lateral parts of the hypoblast grow inwards underneath the axial part, so that the latter (fig. 39, ch) first becomes isolated as an axial cord, and is next inclosed between the medullary cord (nc) (which has by this time been formed) and a continuous sheet of hypoblast below (fig. 40). Here its cells divide and it becomes the notochord. The notochord is thus bodily formed out of the axial portion of the primitive hypoblast. Its mode of origin may be compared with that in Amphioxus, in which an axial fold of the archenteric wall is constricted off as the notochord. The above features in the development of the notochord were first established by Calberla[27] (No. 78).
[27] In Calberla's figure, shewing the development of the notochord, the limits of mesoblast and hypoblast are wrongly indicated.
[FIG. 40. TRANSVERSE SECTION THROUGH PART OF AN EMBRYO OF PETROMYZON PLANERI OF 256 HOURS.
m.c. medullary cord; ch. notochord; al. alimentary canal; ms. mesoblastic plate.]
General history of the development. Up to about the time when the enclosure of the hypoblast by the epiblast is completed, no external traces are visible of any of the organs of the embryo; but about this time, i.e. about 180 hours after impregnation, the rudiment of the medullary plate becomes established, as a linear streak extending forwards from the blastopore over fully one half the circumference of the embryo. The medullary plate first contains a shallow median groove, but it is converted into the medullary cord, not in the usual vertebrate fashion, but, as first shewn by Calberla, in a manner much more closely resembling the formation of the medullary cord in Teleostei. Along the line of the median groove the epiblast becomes thickened and forms a kind of keel projecting inwards towards the hypoblast (fig. 39, nc). This keel is the rudiment of the medullary cord. It soon becomes more prominent, the median groove in it disappears, and it becomes separated from the epiblast as a solid cord (fig. 40, mc).
By this time the whole embryo has become more elongated, and on the dorsal surface is placed a ridge formed by the projection of the medullary cord. At the lip of the blastopore the medullary cord is continuous with the hypoblast, thus forming the rudiment of a neurenteric canal.
Calberla gives a similar account of the formation of the neural canal to that which he gives for the Teleostei (vide p. 72).
He states that the epiblast becomes divided into two layers, of which the outer is involuted into the neural cord, a median slit in the involution representing the neural groove. The eventual neural canal is stated to be lined by the involuted cells. Scott (No. 87) fully confirms Calberla on this point, and, although my own sections do not clearly shew an involution of the outer layer of epiblast cells, the testimony of these two observers must no doubt be accepted on this point.
Shortly after the complete establishment of the neural cord the elongation of the embryo proceeds with great rapidity. The processes in this growth are shewn in fig. 41, A, B, and C. The cephalic portion (A, c) first becomes distinct, forming an anterior protuberance free from yolk. About the time it is formed the mesoblastic plates begin to be divided into somites, but the embryo is so opaque that this process can only be studied in sections. Shortly afterwards an axial lumen appears in the centre of the neural cord, in the same manner as in Teleostei.
The general elongation of the embryo continues rapidly, and, as shewn in my figures, the anterior end is applied to the ventral surface of the yolk (B). With the growth of the embryo the yolk becomes entirely confined to the posterior part. This part is accordingly greatly dilated, and might easily be mistaken for the head. The position of the yolk gives to the embryo a very peculiar appearance. The apparent difference between it and the embryos of other Fishes in the position of the yolk is due in the main to the fact that the postanal portion of the tail is late in developing, and always small. As the embryo grows longer it becomes spirally coiled within the egg-shell. Before hatching the mesoblastic somites become distinctly marked (C).
The hatching takes place at between 13-21 days after impregnation; the period varying according to the temperature.
[FIG. 41. FOUR STAGES IN THE DEVELOPMENT OF PETROMYZON. (After Owsjannikoff.)
c. cephalic extremity; bl. blastopore; op. optic vesicle; au.v. auditory vesicle; br.c. branchial clefts.]
During the above changes in the external form of the embryo, the development of the various organs makes great progress. This is especially the case in the head. The brain becomes distinct from the spinal cord, and the auditory sacks and the optic vesicles of the eye become formed. The branchial region of the mesenteron becomes established, and causes a dilatation of the anterior part of the body, and the branchial pouches grow out from the throat. The anus becomes formed, and a neurenteric canal is also established (Scott). The nature of these and other changes will best be understood by a description of the structure of the just-hatched larva. The general appearance of the larva immediately after hatching is shewn in fig. 41, D. The body is somewhat curved; the posterior extremity being much dilated with yolk, while the anterior is very thin. All the cells still contain yolk particles, which render the embryo very opaque. The larva only exhibits slow movements, and is not capable of swimming about.
The structure of the head is shewn in figs. 42 and 43. Fig. 42 is a section through a very young larva, while fig. 43 is taken from a larva three days after hatching, and shews the parts with considerably greater detail.
[FIG. 42. DIAGRAMMATIC VERTICAL SECTION OF A JUST-HATCHED LARVA OF PETROMYZON. (From Gegenbaur; after Calberla.)
o. mouth; o´. olfactory pit; v. septum between stomodæum and mesenteron; h. thyroid involution; n. spinal cord; ch. notochord; c. heart; a. auditory vesicle.]
On the ventral side of the head is placed the oral opening (fig. 43, m) leading into a large stomodæum which is still without a communication with the mesenteron. Ventrally the stomodæum is prolonged for a considerable distance under the anterior part of the mesenteron. Immediately behind the stomodæum is placed the branchial region of the mesenteron. Laterally it is produced on each side into seven or perhaps eight branchial pouches (fig. 43, br.c), which extend outwards nearly to the skin but are not yet open. Between the successive pouches are placed mesoblastic segments, of the same nature and structure as the walls of the head cavities in the embryos of Elasmobranchs, and like them enclosing a central cavity. A similar structure is placed behind the last, and two similar structures in front of the first persistent pouch. This pouch is situated in the same vertical line as the auditory sack (au.v), and would appear therefore to be the hyobranchial cleft; and this identification is confirmed by the fact of two head cavities being present in front of it. At the front end of the branchial region of the mesenteron is placed a thickened ridge of tissue, which, on the opening of the passage between the stomodæum and the mesenteron, forms a partial septum between the two, and is known as the velum (fig. 43, tv).
[FIG. 43. DIAGRAMMATIC VERTICAL SECTION THROUGH THE HEAD OF A LARVA OF PETROMYZON.
The larva had been hatched three days, and was 4.8 mm. in length. The optic and auditory vesicles are supposed to be seen through the tissues. The letter tv pointing to the base of the velum is where Scott believes the hyomandibular cleft to be situated.
c.h. cerebral hemisphere; th. optic thalamus; in. infundibulum; pn. pineal gland; mb. mid-brain; cb. cerebellum; md. medulla oblongata; au.v. auditory vesicle; op. optic vesicle; ol. olfactory pit; m. mouth; br.c. branchial pouches; th. thyroid involution; v.ao. ventral aorta; ht. ventricle of heart; ch. notochord.]
According to Scott (No. 87) a hyomandibular pouch forming the eighth pouch is formed in front of the pouch already defined as the hyobranchial. It disappears early and does not acquire gill folds[28]. The tissue forming the line of insertion of the velum appears to me to represent the mandibular arch. The grounds for this view are the following:
(1) The structure in question has exactly the position usually occupied by the mandibular arch.
(2) There is present in late larvæ (about 20 days after hatching) an arterial vessel, continued from the ventral prolongation of the bulbus arteriosus along the insertion of the velum towards the dorsal aorta, which has the relations of a true branchial artery.
[28] Scott informs me that he has been unable to find the hyomandibular pouch in larvæ larger than 4.8 mm. My material of the stages when it should be present is somewhat scanty, but I have as yet, very likely owing to the imperfection of my material, been unable to find Scott's hyomandibular pouch either in my sections or surface-views. Huxley describes this pouch as present in the form of a cleft in later stages; I have failed to find his cleft also. The vessel interpreted below as the branchial artery of the mandibular arch was only imperfectly investigated by me, and I was not sure of my interpretations about it. Scott however informs me by letter that it is undoubtedly present.
On the ventral aspect of the branchial region is placed a sack (figs. 42, h, and 43, th), which extends from the front end of the branchial region to the fourth cleft. At first it constitutes a groove opening into the throat above (fig. 44), but soon the opening becomes narrowed to a pore placed between the second and third of the permanent branchial pouches (fig. 43, th). In Ammocoetes[29] the simple tube becomes divided, and assumes a very complicated form, though still retaining its opening into the branchial region of the throat. In the adult it forms a glandular mass underneath the branchial region of the throat equivalent to the thyroid gland of higher Vertebrates.
[29] Schneider (No. 85) states that in the full-grown Ammocoetes the opening is situated between the third and fourth pouches. This is certainly not true for the young larva.
On the ventral aspect of the head, and immediately in front of the mouth, is placed the olfactory pit (fig. 43, ol). It is from the first unpaired, and in just-hatched larvæ simply forms a shallow groove of thickened epiblast at the base of the front of the brain. By the stage represented in fig. 43 the ventral part of the original groove is prolonged into a pit, extending backwards beneath the brain nearly up to the infundibulum.
[FIG. 44. DIAGRAMMATIC TRANSVERSE SECTIONS THROUGH THE BRANCHIAL REGION OF A YOUNG LARVA OF PETROMYZON. (From Gegenbaur; after Calberla.)
d. branchial region of throat.]
On the side of the head, nearly on a level with the front end of the notochord, is placed the eye (fig. 43, op). It is constituted (figs. 45 and 46) of a very shallow optic cup with a thick outer (retinal) layer, and a thin inner choroid layer. In contact with the retinal layer is placed the lens. The latter is formed as an invagination of the skin; to which it is still attached in the just-hatched larva (fig. 45). The eye only differs at this stage from that of other Vertebrata in its extraordinarily small size, and the rudimentary character of its constituent parts.
The auditory sack is a large vesicle (fig. 43, au.v.), placed at the side of the brain opposite the first persistent branchial pouch.
The brain is formed of the usual vertebrate parts[30], but is characterized by the very slight cranial flexure. The fore-brain consists (fig. 43) of a thalamencephalon (th) and an undivided cerebral rudiment (ch). To the roof of the thalamencephalon is attached a flattened sack (pn) which is probably the pineal gland. The floor is prolonged into an infundibulum (in) which contains a prolongation of the third ventricle. The lateral walls of the cerebral rudiment are much thickened.
[30] Max Schultze's statements as to the structure and histology of the brain are very inadequate in the present state of our knowledge.
Behind the thalamencephalon follows the mid-brain (mb), the sides of which form the optic lobes, and behind this again the hind-brain (md); the front border of the roof of which is thickened to form the cerebellum (cb). The medulla passes without any marked line of demarcation into the spinal cord.
[FIG. 45. HORIZONTAL SECTION THROUGH THE HEAD OF A JUST-HATCHED LARVA OF PETROMYZON SHEWING THE DEVELOPMENT OF THE LENS OF THE EYE.
th.c. thalamencephalon; op.v. optic vesicle; l. lens of eye; h.c. head cavity.]
The histological differentiation of the brain has already proceeded to some extent; and it has in the main the same character as the spinal cord. Before the larva has been hatched very long a lateral investment of white matter is present throughout. The notochord (ch) is continued forwards in the head to the hinder border of the infundibulum. It is slightly flexed anteriorly.
From the hinder border of the auditory region to the end of the branchial region the mesoblast is dorsally divided into myotomes, which nearly, though not quite, correspond in number with the branchial pouches.
The growth of the myotomes would seem, as might be anticipated from their independent innervation, not to be related to that of the branchial pouches, so that there is a want of correspondence between these parts, the extent of which varies at different periods of life. The relation between the two in an old larva is shewn in fig. 47.
[FIG. 46. EYE OF A LARVA OF PETROMYZON NINE DAYS AFTER HATCHING.
l. lens; r. retina.
The section passes through one side of the lens.]
The head of the larva of Petromyzon differs very strikingly in general appearance from that of the normal Vertebrata. This is at once shewn by a comparison of fig. 43 with fig. 29. The most important difference between the two is due to the absence of a pronounced cranial flexure in Petromyzon; an absence which is in its turn probably caused by the small development of the fore-brain.
The stomodæum of Petromyzon is surprisingly large, and its size and structure in this type militate against the view of some embryologists that the stomodæum originated from the coalescence of a pair of branchial pouches.
In the region of the trunk there is present an uninterrupted dorsal fin continuous with a ventral fin round the end of the tail.
There is a well-developed body cavity, which is especially dilated in front, in the part which afterwards becomes the pericardium. In this region is placed the nearly straight heart, divided into an auricle and ventricle (figs. 42 and 43), the latter continued forwards into a bulbus arteriosus.
The myotomes are now very numerous (about 57, including those of the head, in a three days' larva). They are separated by septa, but do not fill up the whole space between the septa, and have a peculiar wavy outline. The notochord is provided with a distinct sheath, and below it is placed a subnotochordal rod.
The alimentary canal consists of a narrow anterior section free from yolk, and a posterior region, the walls of which are largely swollen with yolk. The anterior section corresponds to the region of the oesophagus and stomach, but exhibits no distinction of parts. Immediately behind this point the alimentary canal dilates considerably, and on the ventral side is placed the opening of a single large sack, which forms the commencement of the liver. The walls of the hepatic sack are posteriorly united to the yolk-cells. At the region where the hepatic sack opens into the alimentary tract the latter dilates considerably.
The posterior part of the alimentary tract still constitutes a kind of yolk-sack, the ventral wall being enormously thick and formed of several layers of yolk-cells. The dorsal wall is very thin.
The excretory system is composed of two segmental ducts, each connected in front with a well-developed pronephros (head-kidney), with about five ciliated funnels opening into the pericardial region of the body cavity. The segmental ducts in the larvæ open behind into the cloacal section of the alimentary tract.
[FIG. 47. HEAD OF A LARVA OF PETROMYZON SIX WEEKS OLD. (Altered from Max Schultze.)
au.v. auditory vesicle; op. optic vesicle; ol. olfactory pit; ul. upper lip; ll. lower lip; or.p. papillæ at side of mouth; v. velum; br.s. extra branchial skeleton; 1-7. branchial clefts.]
The development of the larva takes place with considerable rapidity. The yolk becomes absorbed and the larva becomes accordingly more transparent. It generally lies upon its side, and resembles in general appearance and habit a minute Amphioxus. It is soon able to swim with vigour, but usually, unless disturbed, is during the day quite quiescent, and chooses by preference the darkest situations. It soon straightens out, and, with the disappearance of the yolk, the tail becomes narrower than the head. A large caudal fin becomes developed.
When the larva is about twenty days old, it bears in most anatomical features a close resemblance to an Ammocoetes; though the histological differences between my oldest larva (29 days) and even very young Ammocoetes are considerable.
The mouth undergoes important changes. The upper lip becomes much more prominent, forming of itself the anterior end of the body (fig. 47, ul). The opening of the nasal pit is in this way relatively thrown back, and at the same time is caused to assume a dorsal position. This will be at once understood by a comparison of fig. 43 with fig. 47. On the inner side of the oral cavity a ring of papillæ is formed (fig. 47, or.p). Dorsally these papillæ are continued forward as a linear streak on the under side of the upper lip. A communication between the oral cavity and the branchial sack is very soon established.
The gill pouches gradually become enlarged; but it is some time before their small external openings are established. Their walls, which are entirely lined by hypoblast, become raised in folds, forming the branchial lamellæ. The walls of the head cavities between them become resolved into the contractors and dilators of the branchial sacks. The extra-branchial basketwork becomes established very early (it is present in the larva of 6 millimetres, about 9 days after hatching) and is shewn in an older larva in fig. 47, br.s. It is not so complicated in these young larvæ as in the Ammocoetes, but in Max Schultze's figure, which I have reproduced, the dorsal elements of the system are omitted. On the dorsal wall of the branchial region a ciliated ridge is formed, which may be homologous with the ridge on the dorsal wall of the branchial sack of Ascidians. It has been described by Schneider in Ammocoetes.
With reference to the remainder of the alimentary canal there is but little to notice. The primitive hepatic diverticulum rapidly sprouts out and forms a tubular gland. The opening into the duodenum changes from a ventral to a lateral or even dorsal position. The duct leads into a gall-bladder imbedded in the substance of the liver. Ventrally the liver is united with the abdominal wall, but laterally passages are left by which the pericardial and body cavities continue to communicate.
The greater part of the yolk becomes employed in the formation of the intestinal wall. This part of the intestine in a nine days' larva (67 mm.) has the form of a cylindrical tube with very thick columnar cells entirely filled with yolk particles. The dorsal wall is no longer appreciably thinner than the ventral. In the later stages the cells of this part of the intestine become gradually less columnar as the yolk is absorbed.
The fate of the yolk-cells in the Lamprey is different from that in most other Vertebrata with an equally large amount of yolk. They no doubt supply nutriment for the growth of the embryo, and although in the anterior part of the intestine they become to some extent enclosed in the alimentary tract and break up, yet in the posterior part they become wholly transformed into the regular epithelium of the intestine.
On the ninth day a slight fold filled with mesoblastic tissue is visible on the dorsal wall of the intestine. This fold appears to travel towards the ventral side; at any rate a similar but better-marked fold is visible in a ventro-lateral position at a slightly later period. This fold is the commencement of the fold which in the adult makes a half spiral, and is no doubt equivalent to the spiral valve of Elasmobranchs and Ganoids. It contains a prolongation of the coeliac artery, which constitutes at first the vitelline artery.
The nervous system does not undergo during the early larval period changes which require a description.
The opening of the olfactory sack becomes narrowed and ciliated (fig. 47, ol). It is carried by the process already mentioned to the dorsal surface of the head. The lumen of the sack is well developed; and lies in contact with the base of the fore part of the brain.
The vascular system presents no very remarkable features. The heart is two-chambered and straight. The ventricle is continued forwards as a bulbus arteriosus, which divides into two arteries at the thyroid body. From the bulbus and its continuations eight branches are given off to the gills; and, as mentioned above, a vessel, probably of the same nature, is given off in the region of the velum. The blood from the branchial sacks is collected into the dorsal aorta. Some of it is transmitted to the head, but the greater part flows backwards under the notochord.
The venous system consists of the usual anterior and posterior cardinal veins which unite on each side into a ductus Cuvieri, and of a great subintestinal vessel of the same nature as that in embryo Elasmobranchs, which persists however in the adult. It breaks up into capillaries in the liver, and constitutes therefore the portal vein. From the liver the blood is brought by the hepatic vein into the sinus venosus. In addition to these vessels there is a remarkable unpaired sub-branchial vein, which brings back the blood directly to the heart from the ventral part of the branchial region.
Metamorphosis. The larva just described does not grow directly into the adult, but first becomes a larval form, known as Ammocoetes, which was supposed to be a distinct species till Aug. Müller (No. 80) made the brilliant discovery of its nature.
The Ammocoetes does not differ to any marked extent from the larva just described. The histological elements become more differentiated, and a few organs reach a fuller development.
The branchial skeleton becomes more developed, and capsules for the olfactory sack and auditory sacks are established.
The olfactory sack is nearly divided into two by a ventral septum. The eye (fig. 48) is much more fully developed, but lies a long way below the surface. The optic cup forms a deep pit, in the mouth of which is placed the lens. The retinal layers are well developed (cf. Langerhans), and the outer layer of the optic cup or layer of retinal pigment (rp) contains numerous pigment granules, especially on its dorsal side. At the edge of the optic cup the two layers fall into each other. They constitute the commencement of the pigment layer of the iris; but at this stage they are not pigmented. The mesoblast of the iris is hardly differentiated. The lens (l) has the normal structure of the embryonic lens of Vertebrata. The inner wall is thick and doubly convex, while the outer wall, which will form the anterior epithelium, is very thin. There is a large space between the lens and the retina containing the vitreous humour (v.h). There is no aqueous humour, and the tissues in front of the lens bear but little resemblance to those in higher Vertebrata. The cornea is represented by (1) the epidermis (ep); (2) the dermis (d.c); (3) the subdermal connective tissue (s.d.c) which passes without any sharp line of demarcation into the dermis; (4) a thick membrane continuous with the choroid which represents Descemet's membrane. The subdermal connective tissue is continued as an investment round the whole eye. There is no specially differentiated sclerotic, and a choroid is only imperfectly indicated[31]. The peculiar features of the eye of the young larva of the Ammocoetes are probably due to degeneration.
[31] Langerhans loc. cit. describes the eye of the Ammocoetes in some respects very differently from the above. Very probably his description applies to an older Ammocoetes. The most important points of difference appear to be (1) that the vitreous humour is all but obliterated; (2) that the iris is much better developed.
[FIG. 48. EYE OF AN AMMOCOETES LYING BENEATH THE SKIN.
ep. epidermis; d.c. dermal connective tissue continuous with the subdermal connective tissue (s.d.c), which is also shaded. There is no definite boundary to this tissue where it surrounds the eye.
m. muscles; dm. membrane of Descemet; l. lens; v.h. vitreous humour; r. retina; rp. retinal pigment.]
In the brain the two cerebral hemispheres lie one on each side of the anterior end of the thalamencephalon. There are well-defined olfactory lobes, and two distinct olfactory nerves are present.
The excretory system has undergone great changes. A series of segmental tubes, which first appear in a larva of about 9 mm., becomes established behind the pronephros, and in an Ammocoetes of 65 mm. the pronephros has begun to atrophy. The generative organs are formed in a larva of about 35 mm. Shortly before the metamorphosis the portion of the cloaca into which the segmental tubes open becomes separated off as a distinct urinogenital sinus, the walls of which become perforated by the two abdominal pores.
The Ammocoetes of Petromyzon Planeri lives in the mud in streams. Without undergoing any marked changes in structure it gradually grows larger, and after three or four years undergoes a metamorphosis. The full-grown larva may be as large or even larger than the adult. The metamorphosis takes place from August till January. The breeding season sets in during the second half of April; and shortly after depositing its generative products the Lamprey dies. The changes which take place in the metamorphosis are of a most striking kind.
The dome-shaped mouth of the larva is replaced (fig. 47) by a more definitely suctorial mouth with horny cuticular teeth (fig. 49). The eyes appear on the surface; and the dorsal fin becomes more prominent, and is divided into two parts.
[FIG. 49. MOUTH OF PETROMYZON MARINUS WITH ITS HORNY TEETH. (From Gegenbaur; after Heckel and Kner.)]
Besides these obvious external changes very great modifications are effected in almost all the organs, which may be very briefly enumerated.
1. Very profound changes take place in the skeleton. An elaborate system of cartilages is developed in connection with the mouth; the cranium itself undergoes important modifications; and neural arches become formed.
2. Considerable changes are effected in the gill pouches, and, according to Schneider, whose statements must however be received with some caution, the branchial sack becomes detached posteriorly from the oesophagus, the oesophagus then sends forwards a prolongation above the branchial sack which is at first solid. This prolongation forms the anterior part of the oesophagus of the adult, and joins the primitive oral cavity at the velum. The so-called bronchus of the adult is thus the whole branchial region of the Ammocoetes, and the anterior part of the oesophagus of the adult is an entirely new formation.
3. The posterior part of the alimentary tract of the Ammocoetes undergoes partial atrophy. The gall-bladder of the liver is absorbed; and the liver itself ceases to communicate with the intestine.
4. The eye undergoes important changes in that it travels to the surface, and acquires all the characters of the normal vertebrate eye.
5. The brain becomes relatively larger but more compact, and the optic lobes (corpora bigemina) become more distinct.
6. The pericardial cavity becomes completely separated from the body cavity, and a distinct pericardium is formed.
7. The mesonephros of the larva disappears, and a fresh posterior part is formed.
Myxine. The ovum of Myxine when ready to be laid is inclosed, as shewn by Allen Thomson[32], in an oval horny shell in many respects similar to that of Elasmobranchii; from its ends there project a number of trumpet-shaped tubular processes, which no doubt serve to attach it to marine objects. No observations have been made on the development.
[32] Cyclopædia of Anat. and Phys. Article 'Ovum.'
BIBLIOGRAPHY.
(77) E. Calberla. "Der Befruchtungsvorgang beim Petromyzon Planeri." Zeit. f. wiss. Zool., Vol. XXX. 1877.
(78) E. Calberla. "Ueb. d. Entwicklung d. Medullarrohres u. d. Chorda dorsalis d. Teleostier u. d. Petromyzonten." Morpholog. Jahrbuch, Vol. III. 1877.
(79) C. Kupffer u. B. Benecke. Der Vorgang d. Befruchtung am Ei d. Neunaugen. Königsberg, 1878.
(80) Aug. Müller. "Ueber die Entwicklung d. Neunaugen." Müller's Archiv, 1856.
(81) Aug. Müller. Beobachtungen üb. d. Befruchtungserscheinungen im Ei d. Neunaugen. Königsberg, 1864.
(82) W. Müller. "Das Urogenitalsystem d. Amphioxus u. d. Cyclostomen." Jenaische Zeitschrift, Vol. IX. 1875.
(83) Ph. Owsjannikoff. "Die Entwick. von d. Flussneunaugen." Vorläuf. Mittheilung. _Mélanges Biologiques tirés du Bulletin de l'Acad. Imp. St Pétersbourg_, Vol. VII. 1870.
(84) Ph. Owsjannikoff. On the development of Petromyzon fluviatilis (Russian).
(85) Anton Schneider. Beiträge z. vergleich. Anat. u. Entwick. d. Wirbelthiere. Quarto. Berlin, 1879.
(86) M. S. Schultze. "Die Entwickl. v. Petromyzon Planeri." Gekrönte Preisschrift. Haarlem, 1856.
(87) W. B. Scott. "Vorläufige Mittheilung üb. d. Entwicklungsgeschichte d. Petromyzonten." Zoologischer Anzeiger, Nos. 63 and 64. III. Jahrg. 1880.
VI. GANOIDEI[33]
[33] The following classification of the Ganoidei is employed in the present chapter:
I. Selachoidei. {Acipenseridæ. {Polyodontidæ.
{Polypteridæ. II. Teleostoidei. {Amiidæ. {Lepidosteidæ.
It is only within quite recent times that any investigations have been made on the embryology of this heterogeneous, but primitive group of fishes. Much still remains to be done, but we now know the main outlines of the development of Acipenser and Lepidosteus, which are representatives of the two important subdivisions of the Ganoids. Both types have a complete segmentation, but Lepidosteus presents in its development some striking approximations to the Teleostei. I have placed at the end of the chapter a few remarks with reference to the affinities indicated by the embryology.
ACIPENSER[34].
[34] Our knowledge of the development of Acipenser is in the main derived from Salensky's valuable observations. His full memoir is unfortunately published in Russian, and I have been obliged to satisfy myself with the abstract (No. 90), and with what could be gathered from his plates. Prof. Salensky very kindly supplied me with some embryos; and I have therefore been able to some extent to work over the subject myself. This is more especially true for the stages after hatching. The embryos of the earlier stages were not sufficiently well preserved for me to observe more than the external features and a few points with reference to the formation of the layers.
The freshly laid ovum is 2 mm. in diameter and is invested by a two-layered shell, covered by a cellular layer derived from the follicle[35]. The segmentation, though complete, approaches the meroblastic type more nearly than the segmentation of the frog's egg. The first furrow appears at the formative pole, at which the germinal vesicle was situated. The earlier phases of the segmentation are like those of meroblastic ova, in that the furrows only penetrate for a certain distance into the egg. Eight vertical furrows appear before the first equatorial furrow; which is somewhat irregular, and situated close to the formative pole.
[35] Seven micropylar apertures, six of which form a circle round the seventh, are stated by Kowalevsky, Wagner, and Owsjannikoff (No. 89) to be present at one of the poles of the inner egg membrane. They are stated by Salensky to vary in number from five to thirteen.
In the later stages the vertical furrows extend through the whole egg, and a segmentation cavity appears between the small and the large spheres. The segmentation is thus in the main similar to that of a frog, from which it diverges in the fact that there is a greater difference in size between the small and the large segments.
[FIG. 50. EMBRYOS OF ACIPENSER VIEWED FROM THE DORSAL SURFACE. (After Salensky.)
A. Stage before the appearance of the mesoblastic somites. B. Stage with five somites.
Mg. medullary groove; bl.p. blastopore; s.d. segmental duct; Fb. fore-brain; Hb. hind-brain; m.s. mesoblastic somite.]
In the final stages of the segmentation the cells become distinctly divided into two layers. A layer of small cells is placed at the formative pole, and constitutes the epiblast. The cells composing it are divided, like those of Teleostei, etc., into a superficial epidermic and a deeper nervous layer. The remaining cells constitute the primitive hypoblast (the eventual hypoblast and mesoblast); they form a great mass of yolk-cells at the lower pole, and also spread along the roof of the segmentation cavity, on the inner side of the epiblast.
A process of unsymmetrical invagination now takes place, which is in its essential features exactly similar to that in the frog or the lamprey, and I must refer the reader for the details of the process to the chapter on the Amphibia. The edge of the cap of epiblast forms an equatorial line. For the greater extent of this line the epiblast cells grow over the hypoblast, as in an epibolic gastrula, but for a small arc they are inflected. At the inflected edge an invagination of cells takes place, underneath the epiblast, towards the segmentation cavity, and gives rise to the dorsal wall of the mesenteron and the main part of the dorsal mesoblast. The slit below the invaginated layer gradually dilates to form the alimentary cavity; the ventral wall of which is at first formed of yolk-cells. The epiblast along the line of the invaginated cells soon becomes thickened, and forms a medullary plate, which is not very distinct in surface views. The cephalic extremity of this plate, which is furthest removed from the edge, dilates, and the medullary plate then assumes a spatula form (fig. 50 A, Mg).
By the continued extension of the epiblast the uncovered part of the hypoblast has in the meantime become reduced to a small circular pore--the blastopore--and in surface views of the embryo has the form represented in fig. 50 A, bl.p. The invagination of the mesenteron has in the meantime extended very far forwards, and the segmentation cavity has become obliterated. The lip of the blastopore has moreover become inflected for its whole circumference.
The invaginated cells forming the dorsal wall of the mesenteron soon become divided into a pigmented hypoblastic epithelium adjoining the lumen of the mesenteron (fig. 51, En) and a mesoblastic layer (Sgp), between the hypoblast and the epiblast. The mesoblast is divided into two plates, between which is placed the notochord[36] (Ch).
[36] Salensky believes that the notochord is derived from the mesoblast. I could not satisfy myself on this point.
With the completion of the medullary plate and the germinal layers, the first embryonic period may be considered to come to a close. The second period ends with the hatching of the embryo. During it the rudiments of the greater number of organs make their appearance. The general form of the embryo during this period is shewn in figs. 50 B and 52 A and B.
One of the first changes to take place is the conversion of the medullary plate into the medullary canal. This, as shewn in fig. 51, is effected in the usual vertebrate fashion, by the establishment of a medullary groove which is then converted into a closed canal by the folding over of the sides.
The uncovered patch of yolk in the blastoporic area soon becomes closed over; and on the formation of the medullary canal the usual neurenteric canal becomes established.
[FIG. 51. TRANSVERSE SECTION THROUGH THE ANTERIOR PART OF AN ACIPENSER EMBRYO. (After Salensky.)
Rf. medullary groove; Mp. medullary plate; Wg. segmental duct; Ch. notochord; En. hypoblast; Sgp. mesoblastic somite; Sp. parietal part of mesoblastic plate.]
The further changes which take place are in the main similar to those in other Ichthyopsida, but in some ways the appearance of the embryo is, as may be gathered from fig. 52, rather strange. This is mainly due to the fact that the embryo does not become folded off from the yolk in the manner usual in Vertebrates; and as will be shewn in the sequel, the relation of the yolk to the embryo is unlike that in any other known Vertebrate. The appearance of the embryo is something like that of an ordinary embryo slit open along the ventral side and then flattened out. Organs which properly belong to the ventral side appear on the lateral parts of the dorsal surface. Owing to the great forward extension of the yolk the heart (fig. 52 B) appears to be placed directly in front of the head.
Even before the formation of the medullary canal the cephalic portion of the nervous system becomes marked out. This part, after the closure of the medullary groove, becomes divided into two (fig. 50 B), and then three lobes--the fore-, the mid-, and the hind-brain (fig. 52, A and B). From the lateral parts of the at first undivided fore-brain the optic vesicles (fig. 52 B, Op) soon sprout out; and in the hind-brain a dilatation to form the fourth ventricle appears in the usual fashion.
[FIG. 52. EMBRYOS OF ACIPENSER BELONGING TO TWO STAGES VIEWED FROM THE DORSAL SURFACE. (After Salensky.)
Fb. fore-brain; Mb. mid-brain; Hb. hind-brain; cp. cephalic plate; Op. optic vesicle; Auv. auditory vesicle; Olp. olfactory pit; Ht. heart; Md. mandibular arch; Ha. hyoid arch; Br´. first branchial arch; Sd. segmental duct.]
The epiblast at the sides of the brain constitutes a more or less well-defined structure, which may be spoken of as a cephalic plate (fig. 52 A, cp). From this plate are formed the essential parts of the organs of special sense. Anteriorly the olfactory pits arise (fig. 52 B, Olp) as invaginations of both layers of the epiblast. The lens of the eye is formed as an ingrowth of the nervous layer only, and opposite the hind-brain the auditory sack (fig. 52 A and B, Auv) is similarly formed from the nervous layer of the epiblast. At the sides of the cephalic plate the visceral arches make their appearance; and in fig. 52 A and B there are shewn the mandibular (Md), hyoid (Ha) and first branchial (Br´) arches, with the hyomandibular (spiracle) and hyobranchial clefts between them. They constitute peculiar concentric circles round the cephalic plate; their shape being due to the flattened form of the embryo, already alluded to.
While the above structures are being formed in the head the changes in the trunk have also been considerable. The mesoblastic plates at the junction of the head and trunk become very early segmented, the segments being formed from before backwards (fig. 50 B). With their formation the trunk rapidly increases in length. At their outer border the segmental duct (fig. 50 B, and fig. 52 A, Sd) is very early established. It is formed, as in Elasmobranchs, as a solid outgrowth of the mesoblast (fig. 51, Wg); but its anterior extremity becomes converted into a pronephros (fig. 57, pr.n).
Before hatching, the embryo has to a small extent become folded off from the yolk both anteriorly and posteriorly; and has also become to some extent vertically compressed. As a result of these changes, the general form of its body becomes much more like that of an ordinary Teleostean embryo.
The general features of the larva after hatching are illustrated by figs. 53, 54 and 55. Fig. 53 represents a larva of about 7 mm. and fig. 54 a lateral and fig. 55 a ventral view of the head of a larva of about 11 mm.
[FIG. 53. LARVA OF ACIPENSER OF 7 MM., SHORTLY AFTER HATCHING.
ol. olfactory pit; op. optic vesicle; sp. spiracle; br.c. branchial clefts; an. anus.]
There are only a few points which call for special attention in the general form of the body. In the youngest larva figured the ventral part of the hyomandibular cleft is already closed: the dorsal part of the cleft is destined to form the spiracle (sp). The arch behind is the hyoid: on its posterior border is a membranous outgrowth, which will develop into the operculum. In older larvæ, a very rudimentary gill appears to be developed on the front walls of the spiracular cleft (Parker), but I have not succeeded in satisfying myself about its presence; and rows of gill papillæ appear on the hyoid and the true branchial arches (figs. 54 and 55, g). The biserially-arranged gill papillæ of the true branchial arches are of considerable length, and are not at first covered by the operculum; but they do not form elongated thread-like external gills similar to those of the Elasmobranchii.
The oral cavity is placed on the ventral side of the head; it has at first a more or less rhomboidal form. It soon however (fig. 55) becomes narrowed to a slit with projecting lips, and eventually becomes converted into the suctorial mouth of the adult. The most remarkable feature connected with the mouth is the development of provisional teeth (fig. 55) on both jaws.
These teeth were first discovered by Knock (No. 88). They do not appear to be calcified, and might be supposed to be of the same nature as the horny teeth of the Lamprey. They are however developed like true teeth, as a deposit between a papilla of subepidermic tissue and an epidermic cap. The substance of which they are formed corresponds morphologically to the enamel of ordinary teeth. As they grow they pierce the epidermis, and form hollow spine-like structures with a central axis filled with subepidermic (mesoblastic) cells. They disappear after the third month of larval life.
In front of the mouth two pairs of papillæ grow out, which appear to be of the same nature as the papillæ on the suctorial disc in the embryo of Lepidosteus (vide p. 115). They are very short in the embryo represented in fig. 53; soon however they grow in length (figs. 54 and 55, st); and it is probable that they become the barbels, since these occupy a precisely similar position[37].
[37] If these identifications are correct the barbels of fishes must be phylogenetically derived from the papillæ of a suctorial disc adjoining the mouth.
[FIG. 54. SIDE VIEW OF A LARVA OF ACIPENSER OF 11 MILLIMETRES.
op. eye; ol. olfactory pit; st. suctorial (?) processes; m. mouth; sp. spiracle; g. gills.]
The openings of the nasal pits are at first single; but the opening of each becomes gradually divided into two by the growth of a flap on the outer side (fig. 54, ol). It is probable that this flap is equivalent to the fold of the superior maxillary process of the Amniota, which by its growth roofs over the open groove which originally leads from the external to the internal nares; so that the two openings of each nasal sack, so established in these and in other fishes, correspond to the external and internal nares of higher Vertebrata.
[FIG. 55. VENTRAL VIEW OF A LARVA OF ACIPENSER OF 11 MILLIMETRES.
m. mouth; st. suctorial (?) processes; op. eye; g. gills.]
At the time of hatching there is a continuous dorso-ventral fin, which, by atrophy in some parts, and hypertrophy in other parts, gives rise to all the unpaired fins of the adult, except the first dorsal and the abdominal. The caudal part of the fin is at first symmetrical, and the heterocercal tail is produced by the special growth of the ventral part of the fin.
[FIG. 56. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE ANTERIOR PART OF THE TRUNK OF A LARVA OF ACIPENSER TO SHEW THE POSITION OCCUPIED BY THE YOLK.
in. intestine; st. stomach filled with yolk; oes. oesophagus; l. liver; ht. heart; ch. notochord; sp.c. spinal cord.]
Of the internal features of development in the Sturgeon the most important concern the relation of the yolk to the alimentary tract. In most Vertebrata the yolk-cells form a protuberance of the part of the alimentary canal, immediately behind the duodenum. The yolk may either, as in the lamprey or frog, form a simple thickening of the alimentary wall in this region, or it may constitute a well-developed yolk-sack as in Elasmobranchii and the Amniota. In either case the liver is placed in front of the yolk. In the Sturgeon on the contrary the yolk is placed almost entirely in front of the liver, and the Sturgeon appears to be also peculiar in that the yolk, instead of constituting an appendage of the alimentary tract, is completely enclosed in a dilated portion of the tract which becomes the stomach (figs. 56 and 57). It dilates this portion to such extent that it might be supposed to form a true external yolk-sack. In the stages before hatching the glandular hypoblast, which was established on the dorsal side of the primitive mesenteron, envelops the yolk-cells, which fuse together into a yolk-mass, and lose all trace of their original cellular structure.
The peculiar flattening out of the embryo over the yolk (vide p. 105) is no doubt connected with the mode in which the yolk becomes enveloped by the hypoblast.
[FIG. 57. TRANSVERSE SECTION THROUGH THE REGION OF THE STOMACH OF A LARVA OF ACIPENSER 5 MM. IN LENGTH.
st. epithelium of stomach; yk. yolk; ch. notochord, below which is a subnotochordal rod; pr.n. pronephros; ao. aorta; mp. muscle-plate formed of large cells, the outer parts of which are differentiated into contractile fibres; sp.c. spinal cord; b.c. body cavity.]
As the posterior part of the trunk, containing the intestine, becomes formed, the yolk is gradually confined to the anterior part of the alimentary tract, which, as before stated, becomes the stomach. The epithelial cells of the stomach, as well as those of the intestine, are enormously dilated with food-yolk (fig. 57, st). Behind the stomach is formed the liver. The subintestinal vein bringing back the blood to the liver appears to have the same course as in Teleostei, in that the blood, after passing through the liver, is distributed to the walls of the stomach and is again collected into a venous trunk which falls into the sinus venosus. As the yolk becomes absorbed, the liver grows forwards underneath the stomach till it comes in close contact with the heart. The relative position of the parts at this stage is shewn diagrammatically in fig. 56. At the commencement of the intestine there arises in the larva of about 14 mm. a great number of diverticula, which are destined to form the compact glandular organ, which opens at this spot in the adult. At this stage there is also a fairly well developed pancreas opening into the duodenum at the same level as the liver.
No trace of the air-bladder was present at the stage in question.
The spiral valve is formed, as in Elasmobranchii, as a simple fold in the wall of the intestine.
There is a well developed subnotochordal rod (fig. 57) which, according to Salensky, becomes the subvertebral ligament of the adult; a statement which confirms an earlier suggestion of Bridge. The pronephros (head-kidney) resembles in the main that of Teleostei (fig. 57); while the front end of the mesonephros, which is developed considerably later than the pronephros, is placed some way behind it. In my oldest larva (14 mm.) the mesonephros did not extend backwards into the posterior part of the abdominal cavity.
BIBLIOGRAPHY.
(88) Knock. "Die Beschr. d. Reise z. Wolga Behufs d. Sterlettbefruchtung." Bull. Soc. Nat. Moscow, 1871.
(89) A. Kowalevsky, Ph. Owsjannikoff, and N. Wagner. "Die Entwick. d. Störe." Vorläuf. Mittheilung. Mélanges Biologiques tirés du Bulletin d. l'Acad. Imp. St Pétersbourg, Vol. VII. 1870.
(90) W. Salensky. "Development of the Sterlet (Acipenser ruthenus)." 2 Parts. Proceedings of the Society of Naturalists in the imperial University of Kasan. 1878 and 9 (Russian). Part I., abstracted in Hoffmann and Schwalbe's Jahresbericht for 1878.
(91) W. Salensky. "Zur Embryologie d. Ganoiden (Acipenser)." Zoologischer Anzeiger, Vol. I., Nos. 11, 12, 13.
LEPIDOSTEUS[38].
[38] Alexander Agassiz was fortunate enough to succeed in procuring and rearing a batch of eggs of this interesting form. He has given an adequate account of the external characters of the post-embryonic stages, and very liberally placed his preserved material of the stages both before and after hatching at Prof. W. K. Parker's and my disposal. The account of the stages prior to hatching is the result of investigations carried on by Professor Parker's son, Mr W. N. Parker, and myself on the material supplied to us by Agassiz. This material was not very satisfactorily preserved, but I trust that our results are not without some interest.
The ova of Lepidosteus are spherical bodies of about 3 mm. in diameter. They are invested by a tough double membrane, composed of (1) an outer layer of somewhat pyriform bodies, radiately arranged, which appear to be the remains of the follicular cells; and (2) of an inner zona radiata, the outer part of which is radiately striated, while the inner part is homogeneous.
[FIG. 58. SURFACE VIEW OF THE OVUM OF LEPIDOSTEUS WITH THE MEMBRANES REMOVED ON THE THIRD DAY AFTER IMPREGNATION.]
The segmentation, as in the Sturgeon, is complete, but approaches closely the meroblastic type. It commences with a vertical furrow at the animal pole, extending through about one-fifth of the circumference. Before this furrow has proceeded further a second furrow is formed at right angles to it. The next stages have not been observed, but on the third day after impregnation (fig. 58), the animal pole is completely divided into small segments, which form a disc similar to the blastoderm of meroblastic ova; while the vegetative pole, which subsequently forms a large yolk-sack, is divided by a few vertical furrows, four of which nearly meet at the pole opposite the blastoderm. The majority of the vertical furrows extend only a short way from the edge of the small spheres, and are partially intercepted by imperfect equatorial furrows.
The stages immediately following the segmentation are still unknown, and in the next stage satisfactorily observed, on the fifth day after impregnation, the body of the embryo is distinctly differentiated. The lower pole of the ovum is then formed of a mass in which no traces of segments or segmentation furrows can be detected.
The embryo (fig. 59) has a dumbbell-shaped outline, and is composed of (1) an outer area, with some resemblance to the area pellucida of an avian embryo, forming the lateral part of the body; and (2) a central portion consisting of the vertebral plates and medullary plate. The medullary plate is dilated in front to form the brain (br). Two lateral swellings in the brain are the commencing optic vesicles. The caudal extremity of the embryo is somewhat swollen.
[FIG. 59. SURFACE VIEW OF A LEPIDOSTEUS EMBRYO ON THE FIFTH DAY AFTER IMPREGNATION.
br. dilated extremity of medullary plate which forms the rudiment of the brain.]
Sections of this stage (fig. 60) are interesting as shewing a remarkable resemblance between Lepidosteus and Teleostei.
The three layers are fully established. The epiblast (ep) is formed of a thicker inner nervous stratum, and an outer flattened epidermic stratum. Along the axial line there is a solid keel-like thickening of the nervous layer of the epidermis, which projects towards the hypoblast. This thickening (MC) is the medullary cord; and there is no evidence of the epidermic layer being at this or any subsequent period concerned in its formation (vide chapter on Teleostei, p. 72). In the region of the brain the medullary cord is so thick that it gives rise, as in Teleostei, to a projection of the whole body of the embryo towards the yolk. Posteriorly it is flatter. The mesoblast (Me) in the trunk has the form of two plates, which thin out laterally. The hypoblast (hy) is a single layer of cells, and is nowhere folded in to form a closed alimentary canal. The hypoblast is separated from the neural cord by the notochord (Ch), which throughout the greater part of the embryo is a distinct structure.
[FIG. 60. SECTION THROUGH AN EMBRYO OF LEPIDOSTEUS ON THE FIFTH DAY AFTER IMPREGNATION.
MC. medullary cord; Ep. epiblast; Me. mesoblast; hy. hypoblast; Ch. notochord.]
In the region of the tail, the axial part of the hypoblast, the notochord, and the neural cord fuse together, the fused part so formed is the homologue of the neurenteric canal of other types. Quite at the hinder end of the embryo the mesoblastic plates cease to be separable from the axial structures between them.
In a somewhat later stage the embryo is considerably more elongated, embracing half the circumference of the ovum. The brain is divided into three distinct vesicles.
Anteriorly the neural cord has now become separated from the epidermis. The whole of the thickened nervous layer of the epiblast appears to remain united with the cerebrospinal cord, so that the latter organ is covered dorsally by the epidermic layer of the epiblast only. The nervous layer soon however grows in again from the two sides.
Where the neural cord is separated from the epidermis, it is already provided with a well-developed lumen. Posteriorly it remains in its earlier condition.
In the region of the hind-brain traces of the auditory vesicles are present in the form of slightly involuted thickenings of the nervous layer of the epidermis.
[FIG. 61. EMBRYO OF LEPIDOSTEUS ON THE SIXTH DAY AFTER IMPREGNATION.
op. optic vesicles; br.c. branchial clefts (?); s.d. segmental duct.
N.B. The branchial clefts and segmental duct are somewhat too prominent.]
The mesoblast of the trunk is divided anteriorly into splanchnic and somatic layers.
In the next stage, on the sixth day after impregnation (fig. 61), there is a great advance in development. The embryo is considerably longer, and a great number of mesoblastic somites are visible. The body is now laterally compressed and raised from the yolk.
The region of the head is more distinct, and laterally two streaks are visible (br.c), which, by comparison with the Sturgeon, would seem to be the two first visceral clefts[39]: they are not yet perforated. In the lateral regions of the trunk the two segmental ducts are visible in surface views (fig. 61, sd) occupying the same situation as in the Sturgeon. Their position in section is shewn in fig. 62, sg.
[39] I have as yet been unable to make out these structures in section.
[FIG. 62. SECTION THROUGH THE TRUNK OF A LEPIDOSTEUS EMBRYO ON THE SIXTH DAY AFTER IMPREGNATION.
mc. medullary cord; ms. mesoblast; sg. segmental duct; ch. notochord; x. subnotochordal rod; hy. hypoblast.]
With reference to the features in development, visible in sections, a few points may be alluded to.
The optic vesicles are very prominent outgrowths of the brain, but are still solid, though the anterior cerebral vesicle has a well-developed lumen. The auditory vesicles are now deep pits of the nervous layer of the epiblast, the openings of which are covered by the epidermic layer. They are shewn for a slightly later stage in fig. 63 (au.v).
There is now present a subnotochordal rod, which develops as in other types from a thickening of the hypoblast (fig. 62, x).
[FIG. 63. SECTION THROUGH THE HEAD OF A LEPIDOSTEUS EMBRYO ON THE SIXTH DAY AFTER IMPREGNATION.
au.v. auditory vesicle; au.n. auditory nerve; ch. notochord; hy. hypoblast.]
In an embryo of the seventh day after impregnation, the features of the preceding stage become generally more pronounced.
The optic vesicles are now provided with a lumen (fig. 64), and have approached close to the epidermis. Adjoining them a thickening (l) of the nervous layer of the epidermis has appeared, which will form the lens. The cephalic extremity of the segmental duct, which, as shewn in fig. 61, is bent inwards towards the middle line, has now become slightly convoluted, and forms the rudiment of a pronephros (head-kidney).
[FIG. 64. SECTION THROUGH THE FRONT PART OF THE HEAD OF A LEPIDOSTEUS EMBRYO ON THE SEVENTH DAY AFTER IMPREGNATION.
al. alimentary tract; fb. thalamencephalon; l. lens of eye; op.v. optic vesicle. The mesoblast is not represented.]
During the next few days the folding off of the embryo from the yolk commences, and proceeds till the embryo acquires the form represented in fig. 65.
Both the head and tail are quite free from the yolk; and the embryo presents a general resemblance to that of a Teleostean.
On the ventral surface of the front of the head there is a disc (figs. 65, 66, sd), which is beset with a number of processes, formed as thickenings of the epiblast. As shewn by Agassiz, these eventually become short suctorial papillæ[40]. Immediately behind this disc is placed a narrow depression which forms the rudiment of the mouth.
[40] These papillæ are very probably sensitive structures; but I have not yet investigated their histological characters.
The olfactory pits are now developed, and are placed near the front of the head.
A great advance has taken place in the development of the visceral clefts and arches. The oral region is bounded behind by a well-marked mandibular arch, which is separated by a shallow depression from a still more prominent hyoid arch (fig. 65, hy). Between the hyoid and mandibular arches a double lamella of hypoblast, which represents the hyomandibular cleft, is continued from the throat to the external skin, but does not, at this stage at any rate, contain a lumen.
The hyoid arch is prolonged backwards into a considerable opercular fold, which to a great extent overshadows the branchial clefts behind. The hyobranchial cleft is widely open.
Behind the hyobranchial cleft are four pouches of the throat on each side, not yet open to the exterior. They are the rudiments of the four branchial clefts of the adult.
The trunk has the usual compressed piscine form, and there is a well-developed dorsal fin continuous round the end of the tail, with a ventral fin. There is no trace of the paired fins.
The anterior and posterior portions of the alimentary tract are closed in, but the middle region is still open to the yolk. The circulation is now fully established, and the vessels present the usual vertebrate arrangement. There is a large subintestinal vein.
[FIG. 65. EMBRYO OF LEPIDOSTEUS SHORTLY BEFORE HATCHING.
ol. olfactory pit; sd. suctorial disc; hy. hyoid arch.]
The first of Agassiz' embryos was hatched about ten days after impregnation. The young fish on hatching immediately used its suctorial disc to attach itself to the sides of the vessel in which it was placed.
[FIG. 66. VENTRAL VIEW OF THE HEAD OF A LEPIDOSTEUS EMBRYO SHORTLY BEFORE HATCHING, TO SHEW THE LARGE SUCTORIAL DISC.
m. mouth; op. eye; s.d. suctorial disc.]
The general form of Lepidosteus shortly after hatching is shewn in fig. 67. On the ventral part of the front of the head is placed the large suctorial disc. At the side of the head are seen the olfactory pit, the eye and the auditory vesicle; while the projecting vesicle of the mid-brain is very prominent above. Behind the mouth follow the visceral arches. The mandibular arch (md) is placed on the hinder border of the mouth, and is separated by a deep groove from the hyoid arch (hy). This groove is connected with the hyomandibular cleft, but I have not determined whether it is now perforated. The posterior border of the hyoid arch is prolonged into an opercular fold. Behind the hyoid arch are seen the true branchial arches.
[FIG. 67. LARVA OF LEPIDOSTEUS SHORTLY AFTER HATCHING. (After Parker.)
ol. olfactory pit; op. optic vesicle; au.v. auditory vesicle; mb. mid-brain; sd. suctorial disc; md. mandibular arch; hy. hyoid arch with operculum; br. branchial arches; an. anus.]
There is still a continuous dorso-ventral fin, in which there are as yet no fin-rays, and the anterior paired fins are present.
The yolk-sack is very large, but its communication with the alimentary canal is confined to a narrow vitelline duct, which opens into the commencement of the intestine immediately behind the duct of the liver, which is now a compact gland. The yolk in Lepidosteus thus behaves very differently from that in the Sturgeon. In the first place it forms a special external yolk-sack, instead of an internal dilatation of part of the alimentary tract; and in the second place it is placed behind instead of in front of the liver.
I failed to find any trace of a pancreas. There is however, opening on the dorsal side of the throat, a well-developed appendage continued backwards beyond the level of the commencement of the intestine. This appendage is no doubt the air-bladder.
In the course of the further growth of the young Lepidosteus, the yolk-sack is rapidly absorbed, and has all but disappeared after three weeks. A rich development of pigment early takes place; and the pigment is specially deposited on the parts of the embryonic fin which will develop into the permanent fins.
The notochord in the tail bends slightly upwards, and by the special development of a caudal lobe an externally heterocercal tail like that of Acipenser is established. The ventral paired fins are first visible after about the end of the third week, and by this time the operculum has grown considerably, and the gills have become well developed.
The most remarkable changes in the later periods are those of the mouth.
[FIG. 68. HEAD OF AN ADVANCED LARVA OF LEPIDOSTEUS. (After Parker.)
ol. openings of the olfactory pit; sd. remains of the larval suctorial disc.]
The upper and lower jaws become gradually prolonged, till they eventually form a snout; while at the end of the upper jaw is placed the suctorial disc, which is now considerably reduced in size (fig. 68, sd). The "fleshy globular termination of the upper jaw of the adult Lepidosteus is the remnant of this embryonic sucking disc." (Agassiz, No. 92.)
The fin-rays become formed as in Teleostei, and parts of the continuous embryonic fin gradually undergo atrophy. The dorsal limb of the embryonic tail, as has been shewn by Wilder, is absorbed in precisely the same manner as in Teleostei, leaving the ventral lobe to form the whole of the permanent tail-fin.
BIBLIOGRAPHY.
(92) Al. Agassiz. "The development of Lepidosteus." Proc. Amer. Acad. of Arts and Sciences, Vol. XIII. 1878.
General observations on the Embryology of the Ganoids.
The very heterogeneous character of the Ganoid group is clearly shewn both in its embryology and its anatomy. The two known types of formation of the central nervous system are exemplified in the two species which have been studied, and these two species, though in accord in having a holoblastic segmentation, yet differ in other important features of development, such as the position of the yolk etc. Both types exhibit Teleostean affinities in the character of the pronephros; but as might have been anticipated Lepidosteus presents in the origin of the nervous system, the relations of the hypoblast, and other characters, closer approximations to the Teleostei than does Acipenser. There are no very prominent Amphibian characters in the development of either type, other than a general similarity in the segmentation and formation of the layers. In the young of Polypterus an interesting amphibian and dipnoid character is found in the presence of a pair of true external gills covered by epiblast. These gills are attached at the hinder end of the operculum, and receive their blood from the hyoid arterial arch[41]. In the peculiar suctorial disc of Lepidosteus, and in the more or less similar structure in the Sturgeon, these fishes retain, I believe, a very primitive vertebrate organ, which has disappeared in the adult state of almost all the Vertebrata; but it is probable that further investigations will shew that the Teleostei, and especially the Siluroids, are not without traces of a similar structure.
[41] Vide Steindachner, Polypterus Lapradei, &c., and Hyrtl, "Ueber d. Blutgefässe, &c." Sitz. Wiener Akad., Vol. LX.
VII. AMPHIBIA[42]
[42] The following classification of the Amphibia is employed in the present chapter: I. Anura. {AGLOSSA. {PHANEROGLOSSA.
{PERENNIBRANCHIATA {Trachystomata. { {Proteidæ. II. Urodela. {CADUCIBRANCHIATA {Amphiumidæ. { {Menopomidæ. {MYCTODERA {Amblystomidæ. {Salamandridæ.
III. Gymnophiona.
The eggs of most Amphibia[43] are laid in water. They are smallish nearly spherical bodies, and in the majority of known Anura (all the European species), and in many Urodela (Amblystoma, Axolotl, though not in the common Newt) part of the surface is dark or black, owing to the presence of a superficial layer of pigment, while the remainder is unpigmented. The pigmented part is at the upper pole of the egg, and contains the germinal vesicle till the time of its atrophy; and the yolk-granules in it are smaller than those in the unpigmented part. The ovum is closely surrounded by a vitelline membrane[44], and receives, in its passage down the oviduct, a gelatinous investment of varying structure.
[43] I am under great obligations to Mr Parker for having kindly supplied me, in answer to my questions, with a large amount of valuable information on the development of the Amphibia.
[44] Within the vitelline membrane there appears to be present, in the Anura at any rate, a very delicate membrane closely applied to the yolk.
In the Anura the eggs are fertilized as they leave the oviduct. In some of the Urodela the mode of fertilization is still imperfectly understood. In Salamanders and probably Newts it is internal[45]; but in Amblystoma punctatum (Clark, No. 98), the male deposits the semen in the water. The eggs are laid by the Anura in masses or strings. By Newts they are deposited singly in the angle of a bent blade of grass or leaf of a water-plant, and by Amblystoma punctatum in masses containing from four eggs to two hundred. Salamandra atra and Salamandra maculosa are viviparous. The period of gestation for the latter species lasts a whole year.
[45] Allen Thomson informs me that he has watched the process of fertilization in the Newt, and that the male deposits the semen in the water close to the female. From the water it seems to enter the female generative aperture. Von Siebold has shewn that there is present in female Newts and Salamanders a spermatic bursa. In this bursa the spermatozoa long (three months) retain their vitality in some Salamanders. Various peculiarities in the gestation are to be explained by this fact.
A good many exceptions to the above general statements have been recorded[46].
[46] For a summary of these and the literature of the subject vide "Amphibia," by C. K. Hoffmann, in Bronn's Classen und Ordnungen d. Thier-reichs.
In Notodelphis ovipara the eggs are transported (by the male?) into a peculiar dorsal pouch of the skin of the female, which has an anterior opening, but is continued backwards into a pair of diverticula. The eggs are very large, and in this pouch, which they enormously distend, they undergo their development. A more or less similar pouch is found in Nototrema marsupiatum.
In the Surinam toad (Pipa dorsigera) the eggs are placed by the male on the back of the female. A peculiar pocket of skin becomes developed round each egg, the open end of which is covered by a gelatinous operculum. The larvæ are hatched, and actually undergo their metamorphosis, in these pockets. The female during this period lives in water. Pipa Americana (if specifically distinct from P. dorsigera) presents nearly the same peculiarities. The female of a tree frog of Ceylon (Polypedates reticulatus) carries the eggs attached to the abdomen.
Rhinoderma Darwinii[47] behaves like some of the Siluroid fishes, in that the male carries the eggs during their development in an enormously developed laryngeal pouch.
[47] Vide Spengel, "Die Fortpflanzung des Rhinoderma Darwinii." Zeit. f. wiss. Zool., Bd. XXIX., 1877. This paper contains a translation of a note by Jiminez de la Espada on the development of the species.
Some Anura do not lay their eggs in water. Chiromantis Guineensis attaches them to the leaves of trees; and Cystignathus mystacius lays them in holes near ponds, which may become filled with water after heavy rains.
The eggs of Hylodes Martinicensis are laid under dead leaves in moist situations.
Formation of the layers.
Anura. The formation of the germinal layers has so far only been studied in some Anura and in the Newt. The following description applies to the Anura, and I have called attention, at the end of the section, to the points in which the Newt is peculiar.
The segmentation of the Frog's ovum has already been described (Vol. II. pp. 95-7), but I may remind the reader that the segmentation (fig. 69) results in the formation of a vesicle, the cavity of which is situated excentrically; the roof of the cavity being much thinner than the floor. The cavity is the segmentation cavity. The roof is formed of two or three layers of smallish pigmented cells, and the floor of large cells, which form the greater part of the ovum. These large cells, which are part of the primitive hypoblast, will be spoken of in the sequel as yolk-cells: they are equivalent to the food-yolk of the majority of vertebrate ova.
[FIG. 69. SEGMENTATION OF COMMON FROG. RANA TEMPORARIA. (After Ecker.)
The numbers above the figures refer to the number of segments at the stage figured.]
The cells forming the roof of the cavity pass without any sharp boundary into the yolk-cells, there being at the junction of the two a number of cells of an intermediate character. The cells both of the roof and the floor continue to increase in number, and those of the roof become divided into two distinct strata (fig. 70, ep).
The upper of these is formed of a single row of somewhat cubical cells, and the lower of several rows of more rounded cells. Both of these strata eventually become the epiblast, of which they form the epidermic and nervous layers. The roof of the segmentation cavity appears therefore to be entirely constituted of epiblast.
The next changes which take place lead (1) to the formation of the mesenteron[48], and (2) to the enclosure of the yolk-cells by the epiblast.
[48] Since the body cavity is not developed as diverticula from the cavity of invagination, the latter cavity may conveniently be called the mesenteron and not the archenteron.
The mesenteron is formed as in Petromyzon and Lepidosteus by an unsymmetrical form of invagination. The invagination first commences by an inflection of the epiblast-cells for a small arc on the equatorial line which marks the junction between the epiblastic cells and the yolk-cells (fig. 70, x).
The inflected cells become continuous with the adjoining cells; and the region where the inflection is formed constitutes a kind of lip, below which a slit-like cavity is soon established. This lip is equivalent to the embryonic rim of the Elasmobranch blastoderm, and the cavity beneath it is the rudiment of the mesenteron.
[FIG. 70. SECTION THROUGH FROG'S OVUM AT THE CLOSE OF SEGMENTATION. (After Götte.)
sg. segmentation cavity; ll. large yolk-containing cells; ep. small cells at formative pole (epiblast); x. point of inflection of epiblast; y. small cells close to junction of the epiblast and yolk.]
The mesenteron now rapidly extends by the invagination of the cells on its dorsal side. These cells grow inwards towards the segmentation cavity as a layer of cells several rows deep. At its inner end, this layer is continuous with the yolk-cells; and is divided into two strata (fig. 71 A), viz. (1) a stratum of several rows of cells adjoining the epiblast, which becomes the mesoblast (m), and (2) a stratum of a single row of more columnar cells lining the cavity of the mesenteron, which forms the hypoblast (hy). The growth inwards of the dorsal wall of the mesenteron is no doubt in part a true invagination, but it seems probable that it is also due in a large measure to an actual differentiation of yolk-cells along the line of growth. The mesenteron is at first a simple slit between the yolk and the hypoblast (fig. 71 A), but as the involution of the hypoblast and mesoblast extends further inwards, this slit enlarges, especially at its inner end, into a considerable cavity; the blind end of which is separated by a narrow layer of yolk-cells from the segmentation cavity (fig. 71 B).
In the course of the involution, the segmentation cavity becomes gradually pushed to one side and finally obliterated. Before obliteration, it appears in some forms (Pelobates fuscus) to become completely enclosed in the yolk-cells.
[FIG. 71. DIAGRAMMATIC LONGITUDINAL SECTIONS THROUGH THE EMBRYO OF A FROG AT TWO STAGES, TO SHEW THE FORMATION OF THE GERMINAL LAYERS. (Modified from Götte.)
ep. epiblast; m. dorsal mesoblast; m´. ventral mesoblast; hy. hypoblast; yk. yolk; x. point of junction of the epiblast and hypoblast at the dorsal side of the blastopore; al. mesenteron; sg. segmentation cavity.]
While the invagination to form the mesenteron takes place as above described, the enclosure of the yolk has been rapidly proceeding. It is effected by the epiblast growing over the yolk at all points of its circumference. The nature of the growth is however very different at the embryonic rim and elsewhere. At the embryonic rim it takes place by the simple growth of the rim, so that the point x in figs. 70 and 71 is carried further and further over the surface of the yolk. Elsewhere the epiblast at first extends over the yolk as in a typical epibolic gastrula, without being inflected to form a definite lip. While a considerable patch of yolk is still left uncovered, the whole of the edge of the epiblast becomes however inflected, as at the embryonic rim (fig. 71 A); and a circular blastopore is established, round the whole edge of which the epiblast and intermediate cells are continuous.
From the ventral lip of the blastopore the mesoblast (fig. 71, m´), derived from the small intermediate cells, grows inwards till it comes to the segmentation cavity; the growth being not so much due to an actual invagination of cells at the lip of the blastopore, as to a differentiation of yolk-cells in situ. Shortly after the stage represented in fig. 71 B, the plug of yolk, which fills up the opening of the blastopore, disappears, and the mesenteron communicates freely with the exterior by a small circular blastopore (fig. 73). The position of the blastopore is the same as in other types, viz. at the hinder end of the embryo.
By this stage the three layers of the embryo are definitely established. The epiblast, consisting from the first of two strata, arises from the small cells forming the roof of the segmentation-cavity. It becomes continuous at the lip of the blastopore with cells intermediate in size between the cells of which it is formed and the yolk-cells. These latter, increasing in number by additions from the yolk-cells, give rise to the mesoblast and to part of the hypoblast; while to the latter layer the yolk-cells, as mentioned above, must also be considered as appertaining. Their history will be dealt with in treating of the general fate of the hypoblast.
Urodela. The early stages of the development of the Newt have been adequately investigated by Scott and Osborn (No. 114). The segmentation and formation of the layers is in the main the same as in the Frog. The ovum is without black pigment. There is a typical unsymmetrical invagination, but the dorsal lip of the blastopore is somewhat thickened. The most striking feature in which the Newt differs from the Frog is the fact that the epiblast is at first constituted of a single layer of cells (fig. 75, ep). The roof of the segmentation cavity is constituted, during the later stages of segmentation, of several rows of cells (Bambeke, No. 95), but subsequently it would appear to be formed of a single row of cells only (Scott and Osborn, No. 114).
General history of the layers.
Epiblast: Anura. At the completion of the invagination the epiblast forms a continuous layer enclosing the whole ovum, and constituted throughout of two strata. The formation of the medullary canal commences by the nervous layer along the axial dorsal line becoming thickened, and giving rise to a somewhat pyriform medullary plate, the sides of which form the projecting medullary folds (fig. 77 A). The medullary plate is thickened at the two sides, and is grooved in the median line by a delicate furrow (fig. 72, r). The dilated extremity of the medullary plate, situated at the end of the embryo opposite the blastopore, is the cerebral part of the plate, and the remainder the spinal. The medullary folds bend upwards, and finally meet above, enclosing a central cerebrospinal canal (fig. 74). The point at which they first meet is nearly at the junction of the brain and spinal cord, and from this point their junction extends backwards and forwards; but the whole process is so rapid that the closure of the medullary canal for its whole length is effected nearly simultaneously. In front the medullary canal ends blindly, but behind it opens freely into the still persisting blastopore, with the lips of which the medullary folds become, as in other types, continuous. Fig. 73 represents a longitudinal section through an embryo, shortly after the closure of the medullary canal (nc); the opening of which into the blastopore (x) is clearly seen.
[FIG. 72. TRANSVERSE SECTION THROUGH THE POSTERIOR CEPHALIC REGION OF AN EARLY EMBRYO OF BOMBINATOR. (After Götte.)
l. medullary groove; r. axial furrow in the medullary groove; h. nervous layer of epidermis; as. outer portion of vertebral plate; is. inner portion of vertebral plate; s. lateral plate of mesoblast; g. notochord; e. hypoblast.]
On the closure of the medullary canal, its walls become separated from the external epiblast, which extends above it as a continuous layer. In the formation of the central nervous system both strata of the epiblast have a share, though the main mass is derived from the nervous layer. After the central nervous tube has become separated from the external skin, the two layers forming it fuse together; but there can be but little doubt that at a later period the epidermic layer separates itself again as the central epithelium of the nervous system.
Both the nervous and epidermic strata have a share in forming the general epiblast; and though eventually they partially fuse together yet the horny layer of the adult epidermis, where such can be distinguished, is probably derived from the epidermic layer of the embryo, and the mucous layer of the epidermis from the embryonic nervous layer.
[FIG. 73. DIAGRAMMATIC LONGITUDINAL SECTION OF THE EMBRYO OF A FROG. (Modified from Götte.)
nc. neural canal; x. point of junction of epiblast and hypoblast at the dorsal lip of the blastopore; al. alimentary tract; yk. yolk-cells; m. mesoblast. For the sake of simplicity the epiblast is represented as if composed of a single row of cells.]
In the formation of the organs of sense the nervous layer shews itself throughout as the active layer. The lens of the eye and the auditory sack are derived exclusively from it, the latter having no external opening. The nervous layer also plays the more important part in the formation of the olfactory sack.
The outer layer of epiblast-cells becomes ciliated after the close of the segmentation, but the cilia gradually disappear on the formation of the internal gills. The cilia cause a slow rotatory movement of the embryo within the egg, and probably assist in the respiration after it is hatched. They are especially developed on the external gills.
Urodela. In the Newt (Scott and Osborn, No. 114) the medullary plate becomes established, while the epiblast is still formed of a single row of cells; and it is not till after the closure of the neural groove that any distinction is observable between the epithelium of the central canal, and the remaining cells of the cerebrospinal cord (fig. 75).
Before the closure of the medullary folds the lateral epiblast becomes divided into the two strata present from the first in the Frog; and in the subsequent development the inner layer behaves as the active layer, precisely as in the Anura.
The mesoblast and notochord: Anura. After the disappearance of the segmentation cavity, the mesoblast is described by most observers, including Götte, as forming a continuous sheet round the ovum, underneath the epiblast. The first important differentiations in it take place, as in the case of the epiblast, in the axial dorsal line. Along this line a central cord of the mesoblast becomes separated from the two lateral sheets to form the notochord. Calberla states, however, that when the mesoblast is distinctly separated from the hypoblast it does not form a continuous sheet, but two sheets one on each side, between which is placed a ridge of cells continuous with the hypoblastic sheet. This ridge subsequently becomes separated from the hypoblast as the notochord. Against this view Götte has recently strongly protested, and given a series of careful representations of his sections which certainly support his original account.
My own observations are in favour of Calberla's statement, and so far as I can determine from my sections the mesoblast never appears as a perfectly continuous sheet, but is always deficient in the dorsal median line. My observations are unfortunately not founded on a sufficient series of sections to settle the point definitely.
[FIG. 74. SECTION THROUGH THE ANTERIOR PART OF THE TRUNK OF A YOUNG EMBRYO OF BOMBINATOR. (After Götte.)
as´´´. medulla oblongata; is^x. splanchnopleure; as^x. somatopleure in the vertebral part of the mesoblastic plate; s. lateral plate of mesoblast; f. throat; e. passage of epithelial cells into yolk-cells; d. yolk-cells; r. dorsal groove along the line of junction of the medullary folds.]
After the formation of the notochord (fig. 72), the mesoblast may be regarded as consisting of two lateral plates, continuous ventrally, but separated in the median dorsal line. By the division of the dorsal parts of these plates into segments, which commences in the region of the neck and thence extends backwards, the mesoblast of the trunk becomes divided into a vertebral portion, cleft into separate somites, and a lateral unsegmented portion (fig. 74).
The history of these two parts and of the mesoblast is generally the same as in Elasmobranchs.
The mesoblast in the head becomes, according to Götte, divided into four segments, equivalent to the trunk somites. Owing to a confusion into which Götte has fallen from not recognizing the epiblastic origin of the cranial nerves, his statements on this head must, I think, be accepted with considerable reserve; but some part of his segments appears to correspond with the head-cavities of Elasmobranchii.
Urodela. Scott and Osborn (No. 114) have shewn that in the Newt the mesoblast (fig. 75) is formed of two lateral plates, split off from the hypoblast, and that the ventral growth of these plates is largely effected by the conversion of yolk-cells into mesoblast-cells. They have further shewn that the notochord is formed of an axial portion of the hypoblast, as in the types already considered (fig. 75). The body cavity is continued into the region of the head; and the mesoblast lining the cephalic section of the body cavity is divided into the same number of head cavities as in Elasmobranchii, viz. one in front of the mouth, and one in the mandibular and one in each of the following arches.
The hypoblast. There are no important points of difference in the relations of the hypoblast between the Anura and Urodela. The mesenteron, at the stage represented in fig. 73, forms a wide cavity lined dorsally by a layer of invaginated hypoblast, and ventrally by the yolk-cells. The hypoblast is continuous laterally and in front with the yolk-cells (figs. 72, 74 and 75). At an earlier stage, when the mesenteron has a less definite form, such a continuity between the true hypoblast and the yolk-cells does not exist at the sides of the cavity.
[FIG. 75. TRANSVERSE SECTION THROUGH THE CEPHALIC REGION OF A YOUNG NEWT EMBRYO. (After Scott and Osborn.)
In.hy. invaginated hypoblast, the dorsal part of which will form the notochord; ep. epiblast of neural plate; sp. splanchnopleure; al. alimentary tract; yk. and Y.hy. yolk-cells.]
The definite closing in of the mesenteron by the true hypoblast-cells commences in front and behind, and takes place last of all in the middle (fig. 76). In front this process takes place with the greatest rapidity. The cells of the yolk-floor become continuously differentiated into hypoblast-cells, and very soon the whole of the front end becomes completely lined by true hypoblastic cells, while the yolk-cells become confined to the floor of the middle part.
The front portion of the mesenteron gives rise to the oesophagus, stomach and duodenum. Close to its hinder boundary there appears a ventral outgrowth, which is the commencement of the hepatic diverticulum (fig. 76, l). The yolk is thus post-hepatic, as in Vertebrates generally.
The stomodæum is formed comparatively late by an epiblastic invagination (fig. 76, m).
[FIG. 76. LONGITUDINAL SECTION THROUGH AN ADVANCED EMBRYO OF BOMBINATOR. (After Götte.)
m. mouth; an. anus; l. liver; ne. neurenteric canal; mc. medullary canal; ch. notochord; pn. pineal gland.]
It should be noticed that the conversion of the yolk-cells into hypoblast-cells to form the ventral wall of the anterior region of the alimentary tract is a closely similar occurrence to the formation of cells in the yolk-floor of the anterior part of the alimentary tract in Elasmobranchii. This conversion is apparently denied by Götte, but since I find cells in all stages of transition between yolk-cells and hypoblast-cells I cannot doubt the fact of its occurrence.
At first, the mesenteron freely communicates with the exterior by the opening of the blastopore. The lips of the blastopore gradually approximate, and form a narrow passage on the dorsal side of which the neural tube opens, as has already been described (fig. 73). The external opening of this passage finally becomes obliterated, and the passage itself is left as a narrow diverticulum leading from the hind end of the mesenteron into the neural canal (fig. 76). It forms the postanal gut, and gradually narrows and finally atrophies. At its front border, on the ventral side, there may be seen a slight ventrally directed diverticulum of the alimentary tract, which first becomes visible at a somewhat earlier stage (fig. 73). This diverticulum becomes longer and meets an invagination of the skin (fig. 76, an), which arises in Rana temporaria at a somewhat earlier period than represented by Götte in Bombinator. This epiblastic invagination is the proctodæum, and an anal perforation eventually appears at its upper extremity.
The differentiation of the hinder end of the præanal gut proceeds in the same fashion as that of the front end, though somewhat later. It gives rise to the cloacal and intestinal part of the alimentary tract. From the ventral wall of the cloacal section, there grows out the bifid allantoic bladder, which is probably homologous with the allantois of the higher Vertebrata. After the differentiation of the ventral wall of the fore and hind ends of the alimentary tract has proceeded for a certain distance, the yolk only forms a floor for a restricted median region of the alimentary cavity, which corresponds to the umbilical canal of the Amniota. The true hypoblastic epithelium then grows over the outer side of the yolk, which thus constitutes a true, though small, and internal yolk-sack. The yolk-cells enclosed in this sack become gradually absorbed, and the walls of the sack form part of the intestine.
General growth of the Embryo.
Anura. The pyriform medullary plate, already described, is the first external indication of the embryo. This plate appears about the stage represented in longitudinal section in fig. 71 B. The feature most conspicuous in it at first is the axial groove. It soon becomes more prominent (fig. 77 A), and ends behind at the blastopore (bl), the lips of which are continuous with the two medullary folds. As the sides of this plate bend upwards to form the closed medullary canal, the embryo elongates itself and assumes a somewhat oval form. At the same time the cranial flexure becomes apparent (fig. 73), and the blastopore shortly afterwards becomes shut off from the exterior. The embryo now continues to grow in length (fig. 77 B), and the mesoblast becomes segmented. The somites are first formed in the neck, and are added successively behind in the unsegmented posterior region of the embryo. The hind end of the embryo grows out into a rounded prominence, which rapidly elongates, and becomes a well-marked tail entirely formed by the elongation of the postanal section of the body. The whole body has a very decided dorsal flexure, the ventral surface being convex. Fig. 78 represents an embryo of Bombinator in side view, with the tail commencing to project. The longitudinal section (fig. 76) is taken through an embryo of about the same age. In the cephalic region important changes have taken place. The cranial flexure has become more marked, but is not so conspicuous a feature in the Amphibia as in most other types, owing to the small size of the cerebral rudiment. The mid-brain is shewn at fig. 78 a forming the termination of the long axis of the body, and the optic vesicles (a´) are seen at its sides.
[FIG. 77. EMBRYOS OF THE COMMON FROG. (After Remak.)
A. Young stage represented enclosed in the egg-membrane. The medullary plate is distinctly formed, but no part of the medullary canal is closed. bl. blastopore.
B. Older embryo after the closure of the medullary canal. oc. optic vesicle. Behind the optic vesicle are seen two visceral arches.]
[FIG. 78. LATERAL VIEW OF AN ADVANCED EMBRYO OF BOMBINATOR. (After Götte.)
a. mid-brain, a´. eye; b. hind-brain; d. mandibular arch; d´. Gasserian ganglion; e. hyoid arch; e´. first branchial arch; f. seventh nerve; f´. glossopharyngeal and vagus nerve; g. auditory vesicle; i. boundary between liver and yolk-sack; k. suctorial disc; l. pericardial prominence; m. prominence formed by the pronephros.]
The rudiments of the mandibular (d), hyoid (e), and first branchial (e´) arches project as folds at the side of the head, but the visceral clefts are not yet open. Rudiments of the proctodæum and stomodæum have appeared, but neither of them as yet communicates with the mesenteron. Below the hyoid arch is seen a peculiar disc (k) which is an embryonic suctorial organ, formed of a plate of thickened epiblast. There is a pair of these discs, one on each side, but only one of them is shewn in the figure. At a later period they meet each other in the middle line, though they separate again before their final atrophy. They are found in the majority of the Anura, but are absent according to Parker in the Aglossa (Pipa and Dactylethra (fig. 83)). They are probably remnants of the same primitive organs as the suctorial disc of Lepidosteus.
[FIG. 79. TRANSVERSE SECTION THROUGH A VERY YOUNG TADPOLE OF BOMBINATOR AT THE LEVEL OF THE ANTERIOR END OF THE YOLK-SACK. (After Götte.)
a. fold of epiblast continuous with the dorsal fin; is^x. neural cord; m. lateral muscle; as^x. outer layer of muscle-plate; s. lateral plate of mesoblast; b. mesentery; u. fold of the peritoneal epithelium which forms the segmental duct; f. alimentary tract; f´. ventral diverticulum which becomes the liver; e. junction of yolk-cells and hypoblast-cells; d. yolk-cells.]
The embryo continues to grow in length, while the tail becomes more and more prominent, and becomes bent round to the side owing to the confinement of the larva within the egg-membrane. At the front of the head the olfactory pits become distinct. The stomodæum deepens, though still remaining blind, and three fresh branchial arches become formed; the last two being very imperfectly differentiated, and not visible from the exterior. There are thus six arches in all, viz. the mandibular, the hyoid and four branchial arches. Between the mandibular and the hyoid, and between each of the following arches, pouches of the mesenteron push their way towards the external skin. Of these pouches there are five, there being no pouch behind the last branchial arch. The first of these will form the hyomandibular cleft, the second the hyobranchial, and the third, fourth and fifth the three branchial clefts.
Although the pouches of the throat meet the external skin, an external opening is not formed in them till after the larva is hatched. Before this takes place there grow, in the majority of forms, from the outer side of the first and second branchial arches small processes, each forming the rudiment of an external gill; a similar rudiment is formed, either before or after hatching, on the third arch; but the fourth arch is without it (figs. 80 and 82).
These external gills, which differ fundamentally from the external gills of Elasmobranchii in being covered by epiblast, soon elongate and form branched ciliated processes floating freely in the medium around the embryo (fig. 80).
Before hatching the excretory system begins to develop. The segmental duct is formed as a fold of the somatic wall at the dorsal side of the body cavity (fig. 79, u). Its anterior end alone remains open to the body cavity, and gives rise to a pronephros with two or three peritoneal openings, opposite to which a glomerulus is formed.
The mesonephros (permanent kidney of Amphibia) is formed as a series of segmental tubes much later than the pronephros, during late larval life. Its anterior end is situated some distance behind the pronephros, and during its formation the pronephros atrophies.
The period of hatching varies in different larvæ, but in most cases, at the time of its occurrence, the mouth has not yet become perforated. The larva, familiarly known as a tadpole, is at first enclosed in the detritus of the gelatinous egg envelopes. The tail, by the development of a dorsal and ventral fin, very soon becomes a powerful swimming organ. Growth, during the period before the larva begins to feed, is no doubt carried on at the expense of the yolk, which is at this time enclosed within the mesenteron.
The mouth and anal perforations are not long in making their appearance, and the tadpole is then able to feed. The gill slits also become perforated, but the hyomandibular diverticulum in most species never actually opens to the exterior, and in all cases becomes very soon closed.
There can be but little doubt that the hyomandibular diverticulum gives rise, as in the Amniota, to the Eustachian tube and tympanic cavity, except when these are absent (i.e. Bombinatoridæ). Götte holds however that these parts are derived from the hyobranchial cleft, but his statements on this head, which would involve us in great morphological difficulties, stand in direct contradiction to the careful researches of Parker.
[FIG. 80. TADPOLES WITH EXTERNAL BRANCHIÆ. (From Huxley; after Ecker.)
A. Lateral view of a young tadpole. B. Ventral view of a somewhat older tadpole.
kb. external branchiæ; m. mouth; n. nasal sack; a. eye; o. auditory vesicle; z. horny jaws; s. ventral sucker; d. opercular fold.
C. More advanced larva, in which the opercular fold has nearly covered the branchiæ.
s. ventral sucker; ks. external branchiæ; y. rudiment of hind limb.]
Shortly after hatching, there grows out from the hyoid arch on each side an opercular fold of skin, which gradually covers over the posterior branchial arches and the external gills (fig. 80 d). It fuses with the skin at the upper part of the gill arches, and also with that of the pericardial wall below them; but is free in the middle, and so assists in forming a cavity, known as the branchial cavity, in which the gills are placed. Each branchial cavity at first opens by a separate widish pore behind (fig. 80), and in Dactylethra both branchial apertures are preserved (Huxley). In the larva of Bombinator, and it would seem also that of Alytes and Pelodytes, the original widish openings of the two branchial chambers meet together in the ventral line, and form a single branchial opening or spiracle. In most other forms, i.e. Rana, Bufo, Pelobates, etc., the two branchial chambers become united by a transverse canal, and the opening of the right sack then vanishes, while that of the left remains as the single unsymmetrical spiracle. In breathing the water is taken in at the mouth, passes through the branchial clefts into the branchial cavities, and is thence carried out by the spiracle.
Immediately after the formation of the branchial cavities, the original external gills atrophy, but in their place fresh gills, usually called internal gills, appear on the outer side of the middle region of the four branchial arches.
There is a single row of these on the first and fourth branchial arches, and two rows on the second and third. In addition to these gills, which are vascular processes of the mesoblast, covered, according to Götte, with an epiblastic (?) epithelium, branchial processes appear on the hypoblastic walls of the three branchial clefts. The last-named branchial processes would appear to be homologous with the gills of Lampreys. In Dactylethra no other gills but these are formed (Parker).
[FIG. 81. TADPOLE OF BOMBINATOR FROM THE VENTRAL SIDE, WITH THE ABDOMINAL WALL REMOVED. (After Götte.)
Behind the mouth are placed the two suckers, and behind these are seen the gills projecting through the spiracles.]
The mouth, even before the tadpole begins to feed, acquires a transversely oval form (fig. 81), and becomes armed with provisional structures in the form of a horny beak and teeth, which are in use during larval life.
The beak is formed of a pair of horny plates moulded on the upper and lower pairs of labial cartilages. The upper valve of the beak is the larger of the two, and covers the lower. The beak is surrounded by a projecting lip formed of a circular fold of skin, the free edge of which is covered by papillæ. Between the papillæ and the beak rows of horny teeth are placed on the inner surface of the lip. There are usually two rows of these on the upper side, the inner one not continuous across the middle line, and three or four rows on the lower side, the inner one or two divided into two lateral parts.
As the tadpole attains its full development, the suctorial organs behind the mouth gradually atrophy. The alimentary canal, which is (fig. 81) at first short, rapidly elongates, and fills up with its numerous coils the large body cavity. In the meantime, the lungs develop as outgrowths from the oesophagus.
Various features in the anatomy of the Tadpole point to its being a repetition of a primitive vertebrate type. The nearest living representative of this type appears to be the Lamprey.
The resemblance between the mouths of the Tadpole and Lamprey is very striking, and many of the peculiarities of the larval skull of the Anura, especially the position of the Meckelian cartilages and the subocular arch, perhaps find their parallel in the skull of the Lamprey[49]. The internal hypoblastic gill-sacks of the Frog, with their branchial processes, are probably equivalent to the gill-sacks of the Lamprey[50]; and it is not impossible that the common posterior openings of the gill-pouches in Myxine are equivalent to the originally paired openings of the branchial sack of the Tadpole.
[49] Vide Huxley, "Craniofacial apparatus of Petromyzon." Journ. of Anat. and Phys. Vol. X. 1876. Huxley's views about the Meckelian arch, etc., are plausible, but it seems probable from Scott's observations that true branchial bars are not developed in the Lamprey. How far this fact necessarily disproves Huxley's views is still doubtful.
[50] Conf. Huxley and Götte.
The resemblances between the Lamprey and the Tadpole appear to me to be sufficiently striking not to be merely the results of more or less similar habits; but at the same time there are no grounds for supposing that the Lamprey itself is closely related to an ancestral form of the Amphibia. In dealing with the Ganoids and other types arguments have been adduced to shew that there was a primitive vertebrate stock provided with a perioral suctorial disc; and of this stock the Cyclostomata are the degraded, but at the same time the nearest living representatives. The resemblances between the Tadpole and the Lamprey are probably due to both of them being descended from this stock. The Ganoids, as we have seen, also shew traces of a similar descent; and the resemblance between the larva of Dactylethra (fig. 83), the Old Red Sandstone Ganoids[51] and Chimæra, probably indicates that an extension of our knowledge will bring to light further affinities between the primitive Ganoid and Holocephalous stocks and the Amphibia.
[51] Cf. Parker (No. 107).
Metamorphosis. The change undergone by the Tadpole in its passage into the Frog is so considerable as to deserve the name of a metamorphosis. This metamorphosis essentially consists in the reduction and atrophy of a series of provisional embryonic organs, and the appearance of adult organs in their place. The stages of this metamorphosis are shewn in fig. 82, 5, 6, 7, 8.
The two pairs of limbs appear nearly simultaneously as small buds; the hinder pair at the junction of the tail and body (fig. 82, 5), and the anterior pair concealed under the opercular membrane. The lungs acquire a greater and greater importance, and both branchial and pulmonary respirations go on together for some time.
[FIG. 82. TADPOLES AND YOUNG OF THE COMMON FROG. (From Mivart.)
1. Recently-hatched Tadpoles twice the natural size. 2. Tadpole with external gills. 2_a_. Same enlarged. 3 and 4. Later stages after the enclosure of the gills by the opercular membrane. 5. Stage with well-developed hind-limbs visible. 6. Stage after the ecdysis, with both pairs of limbs visible. 7. Stage after partial atrophy of the tail. 8. Young Frog.]
When the adult organs are sufficiently developed an ecdysis takes place, in which the gills are completely lost, the provisional horny beak is thrown off, and the mouth loses its suctorial form. The eyes, hitherto concealed under the skin, become exposed on the surface, and the front limbs appear (fig. 82, 6). With these external changes important internal modifications of the mouth, the vascular system, and the visceral arches take place. A gradual atrophy of the tail, commencing at the apex, next sets in, and results in the complete absorption of this organ.
The long alimentary canal becomes shortened, and the, in the main, herbivorous Tadpole gradually becomes converted into the carnivorous Frog (fig. 82, 6, 7, 8).
The above description of the metamorphosis of the Frog applies fairly to the majority of the Anura, but it is necessary to notice a few of the more instructive divergences from the general type.
In the first place, several forms are known, which are hatched in the condition of the adult. The exact amount of metamorphosis which these forms pass through in the egg is still a matter of some doubt. Hylodes Martinicensis is one of these forms. The larva no doubt acquires within the egg a long tail; but while Bavay[52] states that it is provided with external gills, which however are not covered by an operculum, Peters[53] was unable to see any traces of such structures.
[52] Annal. de Sciences Nat., 5th Series, Vol. XVII., 1873.
[53] Berlin. Monatsbericht, 1876, p. 703, and Nature, April 5, 1877.
In Pipa Americana, and apparently in Pipa dorsigera also if a distinct species, the larva leaves the cells on the back of the mother in a condition closely resembling the adult. The embryos of both species develop a long tail in the egg, which is absorbed before hatching, and according to Wyman[54] P. Americana is also temporarily provided with gills, which atrophy early.
[54] Proceed. of Boston Nat. Hist. Society, Vol. V., 1854.
The larva of Rhinoderma Darwinii is stated by Jiminez de la Espada to be without external gills, and it appears to be hatched while still in the laryngeal pouch of the male. In Nototrema marsupiatum the larvæ are also stated to be without external gills.
Amongst the forms with remarkable developments Pseudis paradoxa deserves especial mention, in that the tadpole of this form attains an immensely greater bulk than the adult; a peculiarity which may be simply a question of nutrition, or may perhaps be explained by supposing that the larva resembles a real ancestral form, which was much larger than the existing Frog.
Another form of perhaps still greater morphological interest is the larva of Dactylethra. The chief peculiarities of this larva (fig. 83) have been summarized by Parker (No. 107, p. 626), from whom I quote the following passage:
a. "The mouth is not inferior in position, suctorial and small, but is very wide like that of the 'Siluroids and Lophius;' has an underhung lower jaw, an immensely long tentacle from each upper lip, and possesses no trace of the primordial horny jaws of the ordinary kind.
b. "In conformity with these characters the head is extremely flat or depressed, instead of being high and thick.
c. "There are no claspers beneath the chin.
d. "The branchial orifice is not confined to the left side, but exists on the right side also.
e. "The tail, like the skull, is remarkably chimæroid; it terminates in a long thin pointed lash, and the whole caudal region is narrow and elongated as compared with that of our ordinary Batrachian larvæ.
f. "The fore-limbs are not hidden beneath the opercular fold."
[FIG. 83. LARVA OF DACTYLETHRA. (After Parker.)]
Although most Anurous embryos are not provided with a sufficient amount of yolk to give rise to a yolk-sack as an external appendage of the embryo, yet in some forms a yolk-sack, nearly as large as that of Teleostei, is developed. One of these forms, Alytes obstetricans, belongs to a well-known European genus allied to Pelobates. The embryos of Pipa dorsigera (Parker) are also provided with a very large yolk-sack, round which they are coiled like a Teleostean embryo. A large yolk-sack is also developed in the embryo of Pseudophryne australis.
The actual complexity of the organization of different tadpoles, and their relative size, as compared with the adult, vary considerably. The tadpoles of Toads are the smallest, Pseudophryne australis excelling in this respect; those of Pseudis are the largest known.
The external gills reach in certain forms, which are hatched in late larval stages, a very great development. It seems however that this development is due to these gills being especially required in the stages before hatching. Thus in Alytes, in which the larva leaves the egg in a stage after the loss of the external gills, these structures reach in the egg a very great development. In Notodelphis ovipara, in which the eggs are carried in a dorsal pouch of the mother, the embryos are provided with long vesicular gills attached to the neck by delicate threads. The fact (if confirmed) that some of the forms which are not hatched till post-larval stages are without external gills, probably indicates that there may be various contrivances for embryonic respiration[55]; and that the external gills only attain a great development in those instances in which respiration is mainly carried on by their means. The external gills of Elasmobranchii are probably, as stated in a previous chapter, examples of secondarily developed structures, which have been produced by the same causes as the enlarged gills of Alytes, Notodelphis, etc.
[55] In confirmation of this view it may be mentioned that in Pipa Americana the tail appears to function as a respiratory organ in the later stages of development (Peters).
Urodela. Up to the present time complete observations on the development of the Urodela are confined to the Myctodera[56].
[56] The recent observations on this subject are those of Scott and Osborn (No. 114) on Triton, of Bambeke (No. 95) on various species of Triton and the Axolotl, and of Clark (No. 98) on Amblystoma punctatum.
The early stages are in the main similar to those of the Anura. The body of the embryo is, as pointed out by Scott and Osborn, ventrally instead of dorsally flexed. The metamorphosis is much less complete than in the Anura. The larva of Triton may be taken as typical. At hatching, it is provided with a powerful swimming tail bearing a well-developed fin: there are three pairs of gills placed on the three anterior of the true branchial arches.
Between the hyoid and first branchial arch, and between the other branchial arches, slits are developed, there being four slits in all. At the period just before hatching, only three of these have made their appearance. The hyomandibular cleft is not perforated. Stalked suckers, of the same nature as the suckers of the Anura, are formed on the ventral surface behind the mouth. A small opercular fold, developed from the lower part of the hyoid arch, covers over the bases of the gills. The suctorial mouth and the provisional horny beak of the Anura have no counterpart in these larvæ. The skin is ciliated, and the cilia cause a rotation in the egg. Even before hatching, a small rudiment of the anterior pair of limbs is formed, but the hind-limbs are not developed till a later stage, and the limbs do not attain to any size till the larva is well advanced. In the course of the subsequent metamorphosis lungs become developed, and a pulmonary respiration takes the place of the branchial one. The branchial slits at the same time close and the branchiæ atrophy.
The other types of Myctodera, so far investigated, agree fairly with the Newt.
The larva of Amblystoma punctatum (fig. 84) is provided with two very long processes (s), like the suctorial processes in Triton, placed on the throat in front of the external gills. They are used to support the larva when it sinks to the bottom, and have been called by Clarke (No. 98) balancers. On the development of the limbs, these processes drop off. The external gills atrophy about one hundred days after hatching.
It might have been anticipated that the Axolotl, being a larval form of Amblystoma, would agree in development with Amblystoma punctatum. The conspicuous suctorial processes of the latter form are however represented by the merest rudiments in the Axolotl.
[FIG. 84. LARVÆ OF AMBLYSTOMA PUNCTATUM. (After Clarke.)
n. nasal pit; f. oral invagination; op. eye; s. balancers; f.l. front limb; br. branchiæ.]
The young of Salamandra maculata leave the uterus with external gills, but those of the Alpine Salamander (Salamandra atra) are born in the fully developed condition without gills. In the uterus they pass through a metamorphosis, and are provided (in accordance with the principle already laid down) with very long gill-filaments[57].
[57] Allen Thomson informs me that the crested Newt, Triton cristatus, is in rare instances viviparous.
Salamandra atra has only two embryos, but there are originally a larger number of eggs (Von Siebold), of which all but two fail to develop, while their remains are used as pabulum by the two which survive. Both species of Salamander have a sufficient quantity of food-yolk to give rise to a yolk-sack.
Spelerpes only develops three post-hyoid arches, between which slits are formed as in ordinary types. Menobranchus and Proteus agree with Spelerpes in the number of post-hyoid arches.
One of the most remarkable recent discoveries with reference to the metamorphosis of the Urodela was made by Dumeril[58]. He found that some of the larvæ of the Axolotl, bred in the Jardin des Plantes, left the water, and in the course of about a fortnight underwent a similar metamorphosis to that of the Newt, and became converted into a form agreeing in every particular with the American genus Amblystoma. During this metamorphosis a pulmonary respiration takes the place of a branchial one, the gills are lost, and the gill slits close. The tail loses its fin and becomes rounded, the colour changes, and alterations take place in the gums, teeth, and lower jaw.
[58] Comptes Rendus, 1870, p. 782.
Madame von Chauvin[59] was able, by gradually accustoming Axolotl larvæ to breathe, artificially to cause them to undergo the above metamorphosis.
[59] Zeit. f. wiss. Zool., Bd. XXVII. 1876.
It seems very possible, as suggested by Weismann[60], that the existing Axolotls are really descendants of Amblystoma forms, which have reverted to a lower stage. In favour of this possibility a very interesting discovery of Filippi's[61] may be cited. He found in a pond in a marsh near Andermat some examples of Triton alpestris, which, though they had become sexually mature, still retained the external gills and the other larval characters. Similar sexually mature larval forms of Triton tæniatus have been described by Jullien. These discoveries would seem to indicate that it might be possible artificially to cause the Newt to revert to a perennibranchiate condition.
[60] Zeit. f. wiss. Zool., Bd. XXV. sup. 1875.
[61] Archivio per la Zoologia, l'Anatomia e la Fisiologia, Vol. 1. Genoa, 1861. Conf. also Von Siebold, "Ueber die geschlechtliche Entwicklung d. Urodelen-Larven." Zeit. f. wiss. Zool., Bd. XXVIII., 1877.
Gymnophiona. The development of the Gymnophiona is almost unknown, but it is certain that some larval forms are provided with a single gill-cleft, while others have external gills.
A gill-cleft has been noticed in Epicrium glutinosum (Müller), and in Coecilia oxyura. In Coecilia compressicauda, Peters (No. 108) was unable to find any trace of a gill-cleft, but he observed in the larvæ within the uterus two elongated vesicular gills.
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